Stem cell biomarkers in chronic myeloid leukemia

Disease Markers

Volumn 24, Issue 4-5, 2008, Pages 201-216

  Jiang, Xiaoyan ^a,b   Zhao, Yun ^a   Forrest, Donna ^b   Smith, Clayton ^a,b   Eaves, Allen ^a,b   Eaves, Connie ^a,b  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

BCR ABL targeted therapies; Chronic myeloid leukemia; Drug resistance; Hematopoietic stem cells; Imatinib; Stem cell biomarkers

Indexed keywords

ABC TRANSPORTER; ABLESON HELPER INTEGRATION SITE 1 PROTEIN; BCR ABL PROTEIN; BUSULFAN; CD11B ANTIGEN; CD123 ANTIGEN; CD133 ANTIGEN; CD14 ANTIGEN; CD19 ANTIGEN; CD20 ANTIGEN; CD3 ANTIGEN; CD34 ANTIGEN; CD36 ANTIGEN; CD38 ANTIGEN; CD4 ANTIGEN; CD45RA ANTIGEN; CD56 ANTIGEN; CD61 ANTIGEN; CD66B ANTIGEN; CD71 ANTIGEN; CD8 ANTIGEN; DASATINIB; GLYCOPHORIN A; IMATINIB; INTERFERON; MICROSOMAL AMINOPEPTIDASE; NILOTINIB; THY 1 ANTIGEN; TUMOR MARKER;

ANTIGEN EXPRESSION; AUTOCRINE EFFECT; BLAST CELL CRISIS; CANCER GROWTH; CANCER PATIENT; CANCER STEM CELL; CELL FUNCTION; CELL STRUCTURE; CHRONIC MYELOID LEUKEMIA; CYTOLOGY; GENE EXPRESSION; GENE FUNCTION; GENETIC STABILITY; HEMATOPOIETIC STEM CELL; HUMAN; LEUKEMIA CELL; MULTIPOTENT STEM CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; TREATMENT OUTCOME;

EID: 47849105478     PISSN: 02780240     EISSN: None     Source Type: Journal    
DOI: 10.1155/2008/146871     Document Type: Review

References (146)

1. M. Sattler and J.D. Griffin, Molecular mechanisms of transformation by the BCR-ABL oncogene, Semin Hematol 40 (2003), 4-10.
2. J.V. Melo and M.W. Deininger, Biology of chronic myelogenous leukemia - signaling pathways of initiation and transformation, Hematol Oncol Clin North Am 18 (2004), 545-568.
3. T.G. Lugo, A.M. Pendergast, A.J. Muller and O.N. Witte, Tyrosine kinase activity and transformation potency of bcrabl oncogene products, Science 247 (1990), 1079-1082.
4. bcr/abl gene of the Philadelphia chromosome, Science 247 (1990), 824-830.
5. B.J. Druker, S.Tamura, E. Buchdunger, S. Ohno, G.M. Segal, S. Fanning, J. Zimmermann and N.B. Lydon, Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells, Nat Med 2 (1996), 561-566.
6. B.J. Druker, M. Talpaz, D.J. Resta, B. Peng, E. Buchdunger, J.M. Ford, N.B. Lydon, H. Kantarjian, R. Capdeville, S. Ohno-Jones and C.L. Sawyers, Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia, N Engl J Med 344 (2001), 1031-1037.
7. H. Kantarjian, C. Sawyers, A. Hochhaus, F. Guilhot, C. Schiffer, C. Gambacorti-Passerini, D. Niederwieser, D. Resta, R. Capdeville, U. Zoellner, M. Talpaz, B. Druker, J. Goldman, S.G. O'Brien, N. Russell, T. Fischer, O. Ottmann, P. Cony-Makhoul, T. Facon, R. Stone, C. Miller, M. Tallman, R. Brown, M. Schuster, T. Loughran, A. Gratwohl, F. Mandelli, G. Saglio, M. Lazzarino, D. Russo, M. Baccarani and E. Morra, Hematologic and cytogenetic responses to imatinib mesylate in chronic myelogenous leukemia, N Engl J Med 346 (2002), 645-652.
8. H. Kantarjian, F. Giles, L. Wunderle, K. Bhalla, S. O'Brien, B. Wassmann, C. Tanaka, P. Manley, P. Rae, W. Mietlowski, K. Bochinski, A. Hochhaus, J.D. Griffin, D. Hoelzer, M. Albitar, M. Dugan, J. Cortes, L. Alland, and O.G. Ottmann, Nilotinib in imatinib-resistant CML and Philadelphia chromosome-positive ALL, N Engl J Med 354 (2006), 2542-2551.
9. M. Talpaz, N. P. Shah, H. Kantarjian, N. Donato, J. Nicoll, R. Paquette, J. Cortes, S. O'Brien, C. Nicaise, E. Bleickardt, M.A. Blackwood-Chirchir, V. Iyer, T.T. Chen, F. Huang, A.P. Decillis and C.L. Sawyers, Dasatinib in imatinib-resistant Philadelphia chromosome-positive leukemias, N Engl J Med 354 (2006), 2531-2541.
10. B.J. Druker, F. Guilhot, S.G. O'Brien, I. Gathmann, H. Kantarjian, N. Gattermann, M.W. Deininger, R.T. Silver, J.M. Goldman, R.M. Stone, F. Cervantes, A. Hochhaus, B.L. Powell, J.L. Gabrilove, P. Rousselot, J. Reiffers, J.J. Cornelissen, T. Hughes, H. Agis, T. Fischer, G. Verhoef, J. Shepherd, G. Saglio, A. Gratwohl, J.L. Nielsen, J.P. Radich, B. Simonsson, K. Taylor, M. Baccarani, C. So, L. Letvak and R.A. Larson, Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia, N Engl J Med 355 (2006), 2408-2417.
11. A. Hochhaus and P. La Rosee, Imatinib therapy in chronic myelogenous leukemia: strategies to avoid and overcome resistance, Leukemia 18 (2004), 1321-1331.
12. T. Lahaye, B. Riehm, U. Berger, P. Paschka, M. C. Muller, S. Kreil, K. Merx, U. Schwindel, C. Schoch, R. Hehlmann and A. Hochhaus, Response and resistance in 300 patients with BCR-ABL-positive leukemias treated with imatinib in a single center: a 4. 5-year follow-up, Cancer 103 (2005), 1659-1669.
13. H.M. Kantarjian, M. Talpaz, S. O'Brien, F. Giles, G. Garcia-Manero, S. Faderl, D. Thomas, J. Shan, M.B. Rios and J. Cortes, Dose escalation of imatinib mesylate can overcome resistance to standard-dose therapy in patients with chronic myelogenous leukemia, Blood 101 (2003), 473-475.
14. E. Jabbour, H. Kantarjian, S. O'Brien, M.B. Rios, L. Abruzzo, S. Verstovsek, G. Garcia-Manero and J. Cortes, Sud den blastic transformation in patients with chronic myeloid leukemia treated with imatinib mesylate, Blood 107 (2006), 480-482.
15. H. Kantarjian, S. O'Brien, J. Cortes, F. Giles, D. Thomas, S. Kornblau, J. Shan, R. M. Beth, M. Keating, E. Freireich and M. Talpaz, Sudden onset of the blastic phase of chronic myelogenous leukemia: patterns and implications, Cancer 98 (2003), 81-85.
16. A. Gratwohl, R. Brand, J. Apperley, C. Crawley, T. Ruutu, P. Corradini, E. Carreras, A. Devergie, C. Guglielmi, H.J. Kolb and D. Niederwieser, Allogeneic hematopoietic stem cell transplantation for chronic myeloid leukemia in Europe 2006: transplant activity, long-term data and current results. An analysis by the Chronic Leukemia Working Party of the European Group for Blood and Marrow Transplantation (EBMT), Haematologica 91 (2006), 513-521.
17. J.E. Sokal, E.B. Cox, M. Baccarani, S. Tura, G.A. Gomez, J.E. Robertson, C.Y. Tso, T.J. Braun, B.D. Clarkson, F. Cervantes, C. Rozman and the Italian Cooperative CML Study Group, Prognostic discrimination in "good-risk" chronic granulocytic leukemia, Blood 63 (1984), 789-799.
18. M.E. O'Dwyer, M.J. Mauro, G. Kurilik, M. Mori, S. Balleisen, S. Olson, E. Magenis, R. Capdeville and B.J. Druker, The impact of clonal evolution on response to imatinib mesylate (STI571) in accelerated phase CML, Blood 100 (2002), 1628-1633.
19. J.E. Cortes, M. Talpaz, F. Giles, S. O'Brien, M.B. Rios, J. Shan, G. Garcia-Manero, S. Faderl, D.A. Thomas, W. Wierda, A. Ferrajoli, S. Jeha and H.M. Kantarjian, Prognostic significance of cytogenetic clonal evolution in patients with chronic myelogenous leukemia on imatinib mesylate therapy, Blood 101 (2003), 3794-3800.
20. B.J. Huntly, A. Bench and A.R. Green, Double jeopardy from a single translocation: deletions of the derivative chromosome 9 in chronic myeloid leukemia, Blood 102 (2003), 1160-1168.
21. B.J. Huntly, F. Guilhot, A.G. Reid, G. Vassiliou, E. Hennig, C. Franke, J. Byrne, A. Brizard, D. Niederwieser, J. Freeman-Edward, G. Cuthbert, N. Bown, R.E. Clark, E.P. Nacheva, A.R. Green and M.W. Deininger, Imatinib improves but may not fully reverse the poor prognosis of patients with CML with derivative chromosome 9 deletions, Blood 102 (2003), 2205-2212.
22. A. Quintas-Cardama, H. Kantarjian, M. Talpaz, S. O'Brien, G. Garcia-Manero, S. Verstovsek, M.B. Rios, K. Hayes, A. Glassman, B.N. Bekele, X. Zhou and J. Cortes, Imatinib mesylate therapy may overcome the poor prognostic significance of deletions of derivative chromosome 9 in patients with chronic myelogenous leukemia, Blood 105 (2005), 2281-2286.
23. C.J. Eaves and A.C. Eaves, Progenitor cell dynamics, in: Chronic Myeloid Leukemia: Biology & Treatment, A.M. Carella, G.Q. Daley, C.J. Eaves, J.M. Goldman and R. Hehlmann, eds, Martin Dunitz, 2001, pp. 73-100.
24. T.L. Holyoake, X. Jiang, M.W. Drummond, A.C. Eaves and C.J. Eaves, Elucidating critical mechanisms of deregulated stem cell turnover in the chronic phase of chronic myeloid leukemia, Leukemia 16 (2002), 549-558.
25. S.H. Orkin and L.I. Zon, Hematopoiesis and stem cells: plasticity versus developmental heterogeneity, Nat Immunol 3 (2002), 323-328.
26. S.H. Orkin, Diversification of haematopoietic stem cells to specific lineages, Nat Genet 1 (2000), 57-64.
27. I.L. Weissman, Stem cells: units of development, units of regeneration and units in evolution [In Process Citation], Cell 100 (2000), 157-168.
28. I.L. Weissman, D.J. Anderson and F. Gage, Stem and progenitor cells: origins, phenotypes, lineage commitments and transdifferentiations, Annu Rev Cell Dev Biol 17 (2001), 387-403.
29. C.J. Eaves, Myelopoiesis, in: Leukemia, E.S. Henderson, T.A. Lister and M.F. Greaves, eds, WB Saunders, 2002, pp. 19-45.
30. E. Conneally, J. Cashman, A. Petzer and C. Eaves, Expansion in vitro of transplantable human cord blood stem cells demonstrated using a quantitative assay of their lymphomyeloid repopulating activity in nonobese diabetic-scid/scid mice, Proceedings of the National Academy of Sciences USA 94 (1997), 9836-9841.
31. M. Bhatia, D. Bonnet, U. Kapp, J.C.Y. Wang, B. Murdoch and J.E. Dick, Quantitative analysis reveals expansion of human hematopoietic repopulating cells after short-term ex vivo culture, J Exp Med 186 (1997), 619-624.
32. 2 microglobulin-null mice, J Clin Invest 107 (2001), 199-206.
33. C.J. Hogan, E.J. Shpall and G. Keller, Differential long-term and multilineage engraftment potential from subfractions of human CD34+ cord blood cells transplanted into NOD/SCID mice, Proceedings of the National Academy of Sciences USA 99 (2002), 413-418.
34. J.C.Y. Wang, C. Dorrell, C.Y. Ito, T. Inamitsu, G. Guenechea, O.I. Gan and J.E. Dick, Normal and leukemic human stem cells assayed in immune-deficient mice, in: Hematopoiesis: A Developmental Approach, L.I. Zon, ed., Oxford University Press, 2001, pp. 99-118.
35. B. Dykstra, J. Ramunas, D. Kent, L. McCaffrey, E. Szumsky, L. Kelly, K. Farn, A. Blaylock, C. Eaves and E. Jervis, High-resolution video monitoring of hematopoietic stem cells cultured in single-cell arrays identifies new features of self-renewal, Proceedings of the National Academy of Sciences USA 103 (2006), 8185-8190.
36. X. Jiang, C. Smith, A. Eaves and C. Eaves, The challenges of targeting chronic myeloid leukemia stem cells, Clin Lymph Myeloma 7 (2007), S71-S80.
37. C. Udomsakdi, C.J. Eaves, P.M. Lansdorp and A.C. Eaves, Phenotypic heterogeneity of primitive leukemic hematopoietic cells in patients with chronic myeloid leukemia, Blood 80 (1992), 2522-2530.
38. A.L. Petzer, C.J. Eaves, P.M. Lansdorp, L. Ponchio, M.J. Barnett and A.C. Eaves, Characterization of primitive subpopulations of normal and leukemic cells present in the blood of patients with newly diagnosed as well as established chronic myeloid leukemia, Blood 88 (1996), 2162-2171.
39. M. Bhatia, J.C.Y. Wang, U. Kapp, D. Bonnet and J.E. Dick, Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice, Proceedings of the National Academy of Sciences USA 94 (1997), 5320-5325.
40. C.I. Civin, G. Almeida-Porada, M.-J. Lee, J. Olweus, L.W.M.M. Terstappen and E.D. Zanjani, Sustained, retransplantable, multilineage engraftment of highly purified adult human bone marrow stem cells in vivo, Blood 88 (1996), 4102-4109.
41. - cells home specifically to the bone marrow of NOD/LtSZ scid/scid mice but show different kinetics in expansion, J Immunol 167 (2001), 3692-3698.
42. Y. Yu, A. Flint, E.L. Dvorin and J. Bischoff, AC133-2, a novel isoform of human AC133 stem cell antigen, J Biol Chem 277 (2002), 20711-20716.
43. A. Schulenburg, H. Ulrich-Pur, D. Thurnher, B. Erovic, S. Florian, W.R. Sperr, P. Kalhs, B. Marian, F. Wrba, C.C. Zielinski and P. Valent, Neoplastic stem cells: a novel therapeutic target in clinical oncology, Cancer 107 (2006), 2512-2520.
44. W. Eisterer, X. Jiang, O. Christ, H. Glimm, K. Lee, E. Pang, K. Lambie, G. Shaw, T.L. Holyoake, A.L. Petzer, C. Auewarakul, M.J. Barnett, C.J. Eaves and A.C. Eaves, Different subsets of primary chronic myeloid leukemia stem cells engraft immunodeficient mice and produce a model of the human disease, Leukemia 19 (2005), 435-441.
45. I. Bertoncello, G.S. Hodgson and T.R. Bradley, Multiparameter analysis of transplantable hemopoietic stem cells: I. The separation and enrichment of stem cells homing to marrow and spleen on the basis of Rhodamine-123 fluorescence, Exp Hematol 13 (1985), 999-1006.
46. N.S. Wolf, A. Kone, G.V. Priestley and S.H. Bartelmez, In vivo and in vitro characterization of long-term repopulating primitive hematopoietic cells isolated by sequential Hoechst 33342-rhodamine123 FACS selection, Exp Hematol 21 (1993), 614-622.
47. M.M. Gottesman, T. Fojo and S.E. Bates, Multidrug resistance in cancer: role of ATP-dependent transporters, Nat Rev Cancer 2 (2002), 48-58.
48. S. Zhou, J.D. Scheutz, K.D. Bunting, A.-M. Colapietro, J. Sampath, J.J. Morris, I. Lagutina, G.C. Grosveld, M. Osawa, H. Nakauchi and B.P. Sorrentino, The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype, Nat Med 7 (2001), 1028-1034.
49. M.A. Goodell, K. Brose, G. Paradis, A.S. Conner and R.C. Mulligan, Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo, J Exp Med 183 (1996), 1797-1806.
50. N. Uchida, B. Dykstra, K. Lyons, F. Leung, M. Kristiansen and C. Eaves, ABC transporter activities of murine hematopoietic stem cells vary according to their developmental and activation status, Blood 103 (2004), 4487-4495.
51. C.J. Eaves and A.C. Eaves, Part II. Cell biology and pathobiology. Anatomy and physiology of hematopoiesis, in: Childhood Leukemias, C.-H. Pui, ed., Cambridge University Press, 2006, pp. 69-105.
52. J.L. Mckenzie, K. Takenaka, O.I. Gan, M. Doedens and J.E. Dick, Low rhodamine 123 retention identifies long-term human hematopoietic stem cells within the Lin-CD34+, Blood 109 (2007), 543-545.
53. + side population (SP) phenotype, J Clin Invest 108 (2001), 1071-1077.
54. M. Fischer, M. Schmidt, S. Klingenberg, C.J. Eaves, C. von Kalle and H. Glimm, Short term repopulating cells with myeloid potential in human mobilized peripheral blood do not have a side population (SP) phenotype, Blood 108 (2006), 2121-2123.
55. M. Dean, T. Fojo and S. Bates, Tumour stem cells and drug resistance, Nat Rev Cancer 5 (2005), 275-284.
56. C. Hirschmann-Jax, A.E. Foster, G.G. Wulf, J.G. Nuchtern, T.W. Jax, U. Gobel, M.A. Goodell and M.K. Brenner, A distinct "side population" of cells with high drug efflux capacity in human tumor cells, Proc Natl Acad Sci USA 101 (2004), 14228-14233.
57. C.T. Jordan, D. Upchurch, S.J. Szilvassy, M.L. Guzman, D.S. Howard, A.L. Pettigrew, T. Meyerrose, R. Rossi, B. Grimes, D.A. Rizzieri, S.M. Luger and G.L. Phillips, The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells, Leukemia 14 (2000), 1777-1784.
58. S. Florian, K. Sonneck, A.W. Hauswirth, M.T. Krauth, G.H. Schernthaner, W.R. Sperr and P. Valent, Detection of molecular targets on the surface of CD34+/CD38- stem cells in various myeloid malignancies, Leuk Lymphoma 47 (2006), 207-222.
59. L. Ponchio, E. Conneally and C. Eaves, Quantitation of the quiescent fraction of longterm culture-initiating cells (LTCIC) in normal human blood and marrow and the kinetics of their growth factor-stimulated entry into S-phase in vitro, Blood 86 (1995), 3314-3321.
60. C. Eaves, J. Cashman and A. Eaves, Defective regulation of leukemic hematopoiesis in chronic myeloid leukemia, Leuk Res 22 (1998), 1085-1096.
61. T. Holyoake, X. Jiang, C. Eaves and A. Eaves, Isolation of a highly quiescent subpopulation of primitive leukemic cells in chronic myeloid leukemia, Blood 94 (1999), 2056-2064.
62. T.L. Holyoake, X. Jiang, H.G. Jorgensen, S. Graham, M.J. Alcorn, C. Laird, A.C. Eaves and C.J. Eaves, 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 (2001), 720-728.
63. A. Gratwohl, J. Hermans, D. Niederwieser, F. Frassoni, W. Arcese, G. Gahrton, G. Bandini, E. Carreras, J.P. Vernant, A. Bosi, T. de Witte, W.E. Fibbe, F. Zwaan, M. Michallet, T. Ruutu, A. Devergie, A. Iriondo, J. Apperley, J. Reiffers, B. Speck and J. Goldman, Bone marrow transplantation for chronic myeloid leukemia: long- term results, Bone Marrow Transplant 12 (1993), 509-516.
64. A.S.M.Yong and J.M. Goldman, Relapse of chronic myeloid leukaemia 14 years after allogeneic bone marrow transplantation, Bone Marrow Transplant 23 (1999), 827-828.
65. S.M. Graham, H.G. Jorgensen, E. Allan, C. Pearson, M.J. Alcorn, L. Richmond and T.L. Holyoake, Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro, Blood 99 (2002), 319-325.
66. M. Copland, A. Hamilton, L.J. Elrick, J.W. Baird, E.K. Allan, N. Jordanides, M. Barow, J.C. Mountford and T.L. Holyoake, Dasatinib (BMS-354825) targets an earlier progenitor population than imatinib in primary CML, but does not eliminate the quiescent fraction, Blood 107 (2006), 4532-4539.
67. X. Jiang, A. Lopez, T. Holyoake, A. Eaves and C. Eaves, Autocrine production and action of IL-3 and granulocyte colony-stimulating factor in chronic myeloid leukemia, Proceedings of the National Academy of Sciences USA 96 (1999), 12804-12809.
68. X. Jiang, M. Stuible, Y. Chalandon, A. Li, W. Y. Chan, W. Eisterer, G. Krystal, A. Eaves and C. Eaves, Evidence for a positive role of SHIP in the BCR-ABL-mediated transformation of primitive murine hematopoietic cells and in human chronic myeloid leukemia, Blood 102 (2003), 2976-2984.
69. 1 chromosome, Blood 56 (1980), 356-360.
70. C.J. Eaves, J.D. Cashman, S.D.Wolpe and A.C. Eaves, Unresponsiveness of primitive chronic myeloid leukemia cells to macrophage inflammatory protein 1α, an inhibitor of primitive normal hematopoietic cells, Proceedings of the National Academy of Sciences USA 90 (1993), 12015-12019.
71. J.D. Cashman, C.J. Eaves, A.H. Sarris and A.C. Eaves, MCP-1, not MIP-1α is the endogenous chemokine that cooperates with TGF-β to inhibit the cycling of primitive normal but not leukemic (CML) progenitors in long-term human marrow cultures, Blood 92 (1998), 2338-2344.
72. J.D. Cashman, I. Clark-Lewis, A.C. Eaves and C.J. Eaves, Differentiation stage-specific regulation of primitive human hematopoietic progenitor cycling by exogenous and endogenous inhibitors in an in vivo model, Blood 94 (1999), 3722-3729.
73. J. Cashman, I. Clark-Lewis, A. Eaves and C. Eaves, Stromalderived factor 1 inhibits the cycling of very primitive human hematopoietic cells in vitro and in NOD/SCID mice, Blood 99 (2002), 792-799.
74. J. Cashman, B. Dykstra, I. Clark-Lewis, A. Eaves and C. Eaves, Changes in the proliferative activity of human hematopoietic stem cells in NOD/SCID mice and enhancement of their transplantability after in vivo treatment with cell cycle inhibitors, J Exp Med 196 (2002), 1141-1149.
75. J.D. Cashman, A.C. Eaves and C.J. Eaves, Granulocyte-macrophage colony-stimulating factor modulation of the inhibitory effect of transforming growth factor-β on normal and leukemic human hematopoietic progenitor cells, Leukemia 6 (1992), 886-892.
76. G.K. Sing, J.R. Keller, L.R. Ellingsworth and F.W. Ruscetti, Transforming growth factor β selectively inhibits normal and leukemic human bone marrow cell growth in vitro, Blood 72 (1988), 1504-1511.
77. X. Jiang, Y. Zhao, C. Smith, M. Gasparetto, A. Turhan, A. Eaves and C. Eaves, Chronic myeloid leukemia stem cells possess multiple unique features of resistance to BCR-ABL targeted therapies, Leukemia 21 (2007), 926-935.
78. X. Jiang, K. M. Saw, A. Eaves and C. Eaves, Instability of BCR-ABL Gene in Primary and Cultured Chronic Myeloid Leukemia Stem Cells, J Natl Cancer Inst 99 (2007), 680-693.
79. S. Flamant and A.G. Turhan, Occurrence of de novo ABL kinase domain mutations in primary bone marrow cells after BCR-ABL gene transfer and Imatinib mesylate selection, Leukemia 19 (2005), 1265-1267.
80. M. Koptyra, R. Falinski, M. O. Nowicki, T. Stoklosa, I. Majsterek, M. Nieborowska-Skorska, J. Blasiak and T. Skorski, BCR/ABL kinase induces self-mutagenesis via reactive oxygen species to encode imatinib resistance, Blood 108 (2006), 319-327.
81. C.H. Jamieson, L.E. Ailles, S.J. Dylla, M. Muijtjens, C. Jones, J.L. Zehnder, J. Gotlib, K. Li, M.G. Manz, A. Keating, C.L. Sawyers and I.L. Weissman, Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML, N Engl J Med 351 (2004), 657-667.
82. T. Oda, C. Heaney, J.R. Hagopian, K. Okuda, J.D. Griffin and B.J. Druker, Crkl is the major tyrosine-phosphorylated protein in neutrophils from patients with chronic myelogenous leukemia, J Biol Chem 269 (1994), 22925-22928.
83. + leukemia, Blood 84 (1994), 1731-1736.
84. G.L. Nichols, M.A. Raines, J.C. Vera, L. Lacomis, P. Tempst and D.W. Golde, Identification of CRKL as the constitutively phosphorylated 39-kD tyrosine phosphoprotein in chronic myelogenous leukemia cells, Blood 84 (2004), 2912-2918.
85. D.J. Barnes, D. Palaiologou, E. Panousopoulou, B. Schultheis, A.S. Yong, A. Wong, L. Pattacini, J.M. Goldman and J.V. Melo, Bcr-Abl expression levels determine the rate of development of resistance to imatinib mesylate in chronic myeloid leukemia, Cancer Res 65 (2005), 8912-8919.
86. I.K. Hariharan, J.M. Adams and S. Cory, BCR-ABL oncogene renders myeloid cell line factor independent: Potential autocrine mechanism in chronic myeloid leukemia, Oncogene Res 3 (1988), 387-399.
87. C. Sirard, P. Laneuville and J. Dick, Expression of bcr-abl abrogates factor-dependent growth of human hematopoietic M07E cells by an autocrine mechanism, Blood 83 (1994), 1575-1585.
88. X. Jiang, W. Eisterer, Y. Zhao, N. Harada, C. Porada, G. Almeida-Porada, E. Zanjani, A. Eaves and C. Eaves, Longterm engraftment and persistence of slowly expanding populations of BCR-ABL+ human cells in sheep transplanted in utero 3 years previously with CML cells, Blood 100 (Suppl 1)(2002), 367a.
89. Y. Chalandon, X. Jiang, S. Loutet, A.C. Eaves and C.J. Eaves, Growth autonomy and lineage switching in BCR-ABL-transduced human cord blood cells depend on different functional domains of BCR-ABL, Leukemia 18 (2004), 1006-1012.
90. X. Jiang, E. Ng, C. Yip, W. Eisterer, Y. Chalandon, M. Stuible, A. Eaves and C.J. Eaves, Primitive interleukin 3 null hematopoietic cells transduced with BCR-ABL show accelerated loss after culture of factor-independence in vitro and leukemogenic activity in vivo, Blood 100 (2002), 3731-3740.
91. X. Zhang and R. Ren, BCR-ABL efficiently induces a myeloproliferative disease and production of excess interleukin-3 and granulocyte-macrophage colony-stimulating factor in mice: a novel model for chronic myelogenous leukemia, Blood 92 (1998), 3829-3840.
92. S. Li, R.L. Ilaria, R.P. Million, G.Q. Daley and R.A. Van Etten, The p190, p210 and p230 forms of the BCR/ABL oncogene induce a similar chronic myeloid leukemia-like syndrome in mice but have different lymphoid leukemogenic activity, J Exp Med 189 (1999), 1399-1412.
93. D.G. Peters, K.M. Klucher, R.C. Perlingeiro, S.K. Dessain, E.Y. Koh and G.Q. Daley, Autocrine and paracrine effects of an ES-cell derived, BCR/ABL- transformed hematopoietic cell line that induces leukemia in mice, Oncogene 20 (2001), 2636-2646.
94. P.W. Zandstra, E. Conneally, A.L. Petzer, J.M. Piret and C.J. Eaves, Cytokine manipulation of primitive human hematopoietic cell self-renewal, Proceedings of the National Academy of Sciences USA 94 (1997), 4698-4703.
95. H.G. Jorgensen, M. Copland, E.K. Allan, X. Jiang, A. Eaves, C. Eaves and T.L. Holyoake, Intermittent exposure of primitive quiescent chronic myeloid leukaemia cells to granulocyte colony-stimulating factor in vitro promotes their elimination by imatinib mesylate, Clin Cancer Res 12 (2006), 626-633.
96. Y. Wang, D. Cai, C. Brendel, C. Barett, P. Erben, P.W. Manley, A. Hochhaus, A. Neubauer and A. Burchert, Adaptive secretion of granulocyte-macrophage colony-stimulating factor (GM-CSF) mediates imatinib and nilotinib resistance in BCR/ABL+ progenitors via JAK-2/STAT-5 pathway activation, Blood 109 (2007), 2147-2155.
97. E.R. Lepper, K. Nooter, J. Verweij, M.R. Acharya, W.D. Figg and A. Sparreboom, Mechanisms of resistance to anticancer drugs: the role of the polymorphic ABC transporters ABCB1 and ABCG2, Pharmacogenomics 6 (2005), 115-138.
98. C.W. Scharenberg, M.A. Harkey and B. Torok-Storb, The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors, Blood 99 (2002), 507-512.
99. P.M. Chaudhary and I.B. Roninson, Expression and activity of P-glycoprotein, a multidrug efflux pump, in human hematopoietic stem cells, Cell 66 (1991), 85-94.
100. H. Dai, P. Marbach, M. Lemaire, M. Hayes and W.F. Elmquist, Distribution of STI-571 to the brain is limited by P-glycoprotein-mediated efflux, J Pharmacol Exp Ther 304 (2003), 1085-1092.
101. A. Hamada, H. Miyano, H. Watanabe and H. Saito, Interaction of imatinib mesilate with human P-glycoprotein, J Pharmacol Exp Ther 307 (2003), 824-828.
102. F.X. Mahon, F. Belloc, V. Lagarde, C. Chollet, F. Moreau-Gaudry, J. Reiffers, J.M. Goldman and J.V. Melo, MDR1 gene overexpression confers resistance to imatinib mesylate in leukemia cell line models, Blood 101 (2003), 2368-2373.
103. T. Illmer, M. Schaich, U. Platzbecker, J. Freiberg-Richter, U. Oelschlagel, M. von Bonin, S. Pursche, T. Bergemann, G. Ehninger and E. Schleyer, P-glycoprotein-mediated drug efflux is a resistance mechanism of chronic myelogenous leukemia cells to treatment with imatinib mesylate, Leukemia 18 (2004), 401-408.
104. H. Rumpold, A.M. Wolf, K. Gruenewald, G. Gastl, E. Gunsilius and D. Wolf, RNAi-mediated knockdown of P-glycoprotein using a transposon-based vector system durably restores imatinib sensitivity in imatinib-resistant CML cell lines, Exp Hematol 33 (2005), 767-775.
105. N.Widmer, S. Colombo, T. Buclin and L.A. Decosterd, Functional consequence of MDR1 expression on imatinib intracellular concentrations, Blood 102 (2003), 1142.
106. P.T. Ferrao, M.J. Frost, S.P. Siah and L.K. Ashman, Overexpression of P-glycoprotein in K562 cells does not confer resistance to the growth inhibitory effects of imatinib (STI571) in vitro, Blood 102 (2003), 4499-4503.
107. Y. Zong, S. Zhou and B.P. Sorrentino, Loss of P-glycoprotein expression in hematopoietic stem cells does not improve responses to imatinib in a murine model of chronic myelogenous leukemia, Leukemia 19 (2005), 1590-1596.
108. P.J. Houghton, G.S. Germain, F.C. Harwood, J.D. Schuetz, C.F. Stewart, E. Buchdunger and P. Traxler, Imatinib mesylate is a potent inhibitor of the ABCG2 (BCRP) transporter and reverses resistance to topotecan and SN-38 in vitro, Cancer Res 64 (2004), 2333-2337.
109. H. Burger, H. van Tol, A. W. Boersma, M. Brok, E.A. Wiemer, G. Stoter and K. Nooter, Imatinib mesylate (STI571) is a substrate for the breast cancer resistance protein (BCRP)/ABCG2 drug pump, Blood 104 (2004), 2940-2942.
110. H. Burger, H. van Tol, M. Brok, E.A.Wiemer, E.A. de Bruijn, G. Guetens, G. de Boeck, A. Sparreboom, J. Verweij and K. Nooter, Chronic imatinib mesylate exposure leads to reduced intracellular drug accumulation by induction of the ABCG2 (BCRP) and ABCB1 (MDR1) drug transport pumps, Cancer Biol Ther 4 (2005), 747-752.
111. T. Nakanishi, K. Shiozawa, B.A. Hassel and D.D. Ross, Complex interaction of BCRP/ABCG2 and imatinib in BCR-ABL-expressing cells: BCRP-mediated resistance to imatinib is attenuated by imatinib-induced reduction of BCRP expression, Blood 108 (2006), 678-684.
112. N.E. Jordanides, H.G. Jorgensen, T.L. Holyoake and J.C. Mountford, Functional ABCG2 is over-expressed on primary CML CD34+ cells and is inhibited by imatinib mesylate, Blood 108 (2006), 1370-1373.
113. A.H. Schinkel, U. Mayer, E. Wagenaar, C.A. Mol, L. van Deemter, J.J. Smit, M.A. van der Valk, A.C. Voordouw, H. Spits, O. van Tellingen, J.M. Zijlmans, W.E. Fibbe and P. Borst, Normal viability and altered pharmacokinetics in mice lacking mdr1-type (drug-transporting) P-glycoproteins, Proceedings of the National Academy of Sciences USA 94 (1997), 4028-4033.
114. S. Zhou, J.J. Morris, Y. Barnes, L. Lan, J.D. Schuetz and B.P. Sorrentino, Bcrp1 gene expression is required for normal numbers of side population stem cells in mice and confers relative protection to mitoxantrone in hematopoietic cells in vivo, Proceedings of the National Academy of Sciences USA 99 (2002), 12339-12344.
115. D.L. White, V.A. Saunders, P. Dang, J. Engler, A.C. Zannettino, A.C. Cambareri, S.R. Quinn, P.W. Manley and T.P. Hughes, OCT-1 mediated influx is a key determinant of the intracellular uptake of imatinib but not nilotinib (AMN107); reduced OCT-1 activity is the cause of low in vitro sensitivity to imatinib, Blood 108 (2006), 697-704.
116. J. Thomas, L.Wang, R.E. Clark and M. Pirmohamed, Active transport of imatinib into and out of cells: implications for drug resistance, Blood 104 (2004), 3739-3745.
117. L.C. Crossman, B.J. Druker, M.W. Deininger, M. Pirmohamed, L. Wang and R.E. Clark, hOCT 1 and resistance to imatinib, Blood 106 (2005), 1133-1134.
118. X. Jiang, Z. Hanna, M. Kaouass, L. Girard and P. Jolicoeur, Ahi-1, a novel gene encoding a modular protein with WD40-repeat and SH3 domains, is targeted by the Ahi-1 and Mis-2 provirus integrations, J Virol 76 (2002), 9046-9059.
119. Y. Poirier, C.A. Kozak and P. Jolicoeur, Identification of a common helper provirus integration site in Abelson murine leukemia virus-induced lymphoma DNA, J Virol 62 (1988), 3985-3992.
120. L. Villeneuve, X. Jiang, C. Turmel, C.A. Kozak and P. Jolicoeur, Long-range mapping of Mis-2, a common provirus integration site identified in murine leukemia virus-induced thymomas and located 160 kilobase pairs downstream of Myb, J Virol 67 (1993), 5733-5739.
121. D/myc transgenic mice suggests a collaboration of c-myc and Notch1 for oncogenesis, Genes Dev 10 (1996), 1930-1944.
122. Y. Haupt, W.S. Alexander, G. Barri, S.P. Klinken and J.M. Adams, Novel zinc finger gene implicated as myc collaborator by retrovirally accelerated lymphomagenesis in Exuu-myc transgenic mice, Cell 65 (1991), 753-763.
123. M. van Lohuizen, S. Verbeek, B. Scheijen, E. Wientjens, H. van der Gulden and A. Berns, Identification of cooperating oncogenes in E mu-myc transgenic mice by provirus tagging, Cell 65 (2002), 737-752.
124. S.M. Blaydes, S.C. Kogan, B.T. Truong, D.J. Gilbert, N.A. Jenkins, N.G. Copeland, D.A. Largaespada and C.I. Brannan, Retroviral integration at the Epil locus cooperates with Nfl gene loss in the progression to acute myeloid leukemia, J Virol 75 (2001), 9427-9434.
125. +human leukemias of AHI-1, a gene activated by insertional mutagenesis in mouse models of leukemia, Blood 103 (2004), 3897-3904.
126. L. Zhou, A. Ringrose, A.E.-J. Lin and X. Jiang, Deregulated expression of a novel oncogene, Ahi-1, in murine hematopoietic cells confers a proliferative advantage in vitro and leukemogenic activity in vivo and enhances the effects of BCR-ABL, Blood 108 (Suppl 1)(2006), 119a.
127. + hematopoietic stem and progenitor cells in chronic myelogenous leukemia, Oncogene 24 (2005), 5313-5324.
128. E. Diaz-Blanco, I. Bruns, F. Neumann, J. C. Fischer, T. Graef, M. Rosskopf, B. Brors, S. Pechtel, S. Bork, A. Koch, A. Baer, U.P. Rohr, G. Kobbe, A. Haeseler, N. Gattermann, R. Haas and R. Kronenwett, Molecular signature of CD34(+) hematopoietic stem and progenitor cells of patients with CML in chronic phase, Leukemia 21 (2007), 494-504.
129. E.T. Penserga and T. Skorski, Fusion tyrosine kinases: a result and cause of genomic instability, Oncogene 26 (2007), 11-20.
130. T. Skorski, Oncogenic tyrosine kinases and the DNA-damage response, Nat Rev Cancer 2 (2002), 351-360.
131. C.M. Verfaillie, J.B. McCarthy and P.B. McGlave, Mechanisms underlying abnormal trafficking of malignant progenitors in chronic myelogenous leukemia, J Clin Invest 90 (1992), 1232-1241.
132. R. Salgia, E. Quackenbush, J. Lin, N. Souchkova, M. Sattler, D.S. Ewaniuk, K.M. Klucher, G.Q. Daley, S.K. Kraeft, R. Sackstein, E.P. Alyea III, U.H. von Andrian, L.B. Chen, J.-C. Gutierrez-Ramos, A.-M. Pendergast and J.D. Griffin, The BCR/ABL oncogene alters the chemotactic response to stromal-derived factor-1α, Blood 94 (1999), 4233-4246.
133. S. Ghaffari, G.J. Dougherty, P.M. Lansdorp, A.C. Eaves and C.J. Eaves, Differentiation - associated changes in CD44 isoform expression during normal hematopoiesis and their alteration in chronic myeloid leukemia, Blood
134. D.S. Krause, K. Lazarides, U.H. von Andrian and R.A. Van Etten, Requirement for CD44 in homing and engraftment of BCR-ABL-expressing leukemic stem cells, Nat Med 12 (2006), 1175-1180.
135. T. Holtschke, J. Lohler, Y. Kanno, T. Fehr, N. Giese, F. Rosenbauer, J. Lou, K.P. Knobeloch, L. Gabriele, J.F. Waring, M.F. Bachmann, R.M. Zinkernagel, H.C. Morse III, K. Ozato and I. Horak, Immunodeficiency and chronic myelogenous leukemia-like syndrome in mice with a targeted mutation of the ICSBP gene, Cell 87 (1996), 307-317.
136. S.X. Hao and R. Ren, Expression of interferon consensus sequence binding protein (ICSBP) is downregulated in Bcr-Abl-induced murine chronic myelogenous leukemia-like disease and forced coexpression of ICSBP inhibits Bcr-Abl-induced myeloproliferative disorder, Mol Cell Biol 20 (2000), 1149-1161.
137. U. Steidl, S. Bork, S. Schaub, O. Selbach, J. Seres, M. Aivado, T. Schroeder, U.P. Rohr, R. Fenk, S. Kliszewski, C. Maercker, P. Neubert, S.R. Bornstein, H.L. Haas, G. Kobbe, D.G. Tenen, R. Haas and R. Kronenwett, Primary human CD34+ hematopoietic stem and progenitor cells express functionally active receptors of neuromediators, Blood 104 (2004), 81-88.
138. D. Soligo, F. Servida, D. Delia, E. Fontanella, G. Lamorte, L. Caneva, R. Fumiatti and D.G. Lambertenghi, The apoptogenic response of human myeloid leukaemia cell lines and of normal and malignant haematopoietic progenitor cells to the proteasome inhibitor PSI, Br J Haematol 113 (2001), 126-135.
139. F. Servida, D. Soligo, D. Delia, C. Henderson, C. Brancolini, L. Lombardi and G.L. Deliliers, Sensitivity of human multiple myelomas and myeloid leukemias to the proteasome inhibitor I, Leukemia 19 (2005), 2324-2331.
140. S. Salesse and C.M. Verfaillie, BCR/ABL-mediated increased expression of multiple known and novel genes that may contribute to the pathogenesis of chronic myelogenous leukemia, Mol Cancer Ther 2 (2003), 173-182.
141. D.H. Lam and P.D. Aplan, NUP98 gene fusions in hematologic malignancies, Leukemia 15 (2001), 1689-1695.
142. L.A. McLean, I. Gathmann, R. Capdeville, M.H. Polymeropoulos and M. Dressman, Pharmacogenomic analysis of cytogenetic response in chronic myeloid leukemia patients treated with imatinib, Clin Cancer Res 10 (2004), 155-165.
143. O. Frank, B. Brors, A. Fabarius, L. Li, M. Haak, S. Merk, U. Schwindel, C. Zheng, M.C. Muller, N. Gretz, R. Hehlmann, A. Hochhaus and W. Seifarth, Gene expression signature of primary imatinib-resistant chronic myeloid leukemia patients, Leukemia 20 (2006), 1400-1407.
144. R. Villuendas, J.L. Steegmann, M. Pollan, L. Tracey, A. Granda, E. Fernandez-Ruiz, L.F. Casado, J. Martinez, P. Martinez, L. Lombardia, L. Villalon, J. Odriozola and M.A. Piris, Identification of genes involved in imatinib resistance in CML: a gene-expression profiling approach, Leukemia 20 (2006), 1047-1054.
145. + cells identifies low expression of CD7, along with high expression of proteinase 3 or elastase, as predictors of longer survival in patients with CML, Blood 107 (2006), 205-212.
146. + bone marrow cells, Stem Cells 25 (2007), 1681-1689.