The bone marrow microenvironment as a sanctuary for minimal residual disease in CML

Biochemical Pharmacology

Volumn 80, Issue 5, 2010, Pages 602-612

  Nair, Rajesh R ^a   Tolentino, Joel ^a   Hazlehurst, Lori A ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

BCR ABL; CAM DR; Cancer stem cell; Chronic myeloid leukemia; Drug resistance; Tumor microenvironment

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 MORPHOLINO 8 PHENYLCHROMONE; ALPHA INTERFERON; BORTEZOMIB; CYCLOPROPANECARBOXYLIC ACID [4 [4 (4 METHYL 1 PIPERAZINYL) 6 (5 METHYL 2H PYRAZOL 3 YLAMINO) 2 PYRIMIDINYLTHIO]PHENYL]AMIDE; CYCLOSPORIN A; CYTARABINE; DANUSERTIB; DASATINIB; DCC 2036; EVEROLIMUS; GNF 2; GNF 5; IMATINIB; LFA 703; LONAFARNIB; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; NILOTINIB; PANOBINOSTAT; PD 18435273; PLERIXAFOR; PROTEIN TYROSINE KINASE INHIBITOR; TIPIFARNIB; UNCLASSIFIED DRUG; VALPROIC ACID; VORINOSTAT;

BONE MARROW CELL; CANCER CHEMOTHERAPY; CANCER STEM CELL; CHRONIC MYELOID LEUKEMIA; CLINICAL TRIAL; DRUG EFFICACY; DRUG TARGETING; EXTRACELLULAR MATRIX; HEMATOPOIETIC STEM CELL; HUMAN; MINIMAL RESIDUAL DISEASE; MULTIDRUG RESISTANCE; NONHUMAN; OSTEOBLAST; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW;

BONE MARROW; DRUG RESISTANCE, NEOPLASM; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; NEOPLASM, RESIDUAL; NEOPLASTIC STEM CELLS;

EID: 77954219134     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2010.04.003     Document Type: Review

References (174)

1. Rowley J.D. Letter: a new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature 1973, 243:290-293.
2. Bartram C.R., de Klein A., Hagemeijer A., van Agthoven T., Geurts van Kessel A., Bootsma D., et al. Translocation of c-ab1 oncogene correlates with the presence of a Philadelphia chromosome in chronic myelocytic leukaemia. Nature 1983, 306:277-280.
3. Heisterkamp N., Stephenson J.R., Groffen J., Hansen P.F., de Klein A., Bartram C.R., et al. Localization of the c-ab1 oncogene adjacent to a translocation break point in chronic myelocytic leukaemia. Nature 1983, 306:239-242.
4. Sattler M., Griffin J.D. Molecular mechanisms of transformation by the BCR-ABL oncogene. Semin Hematol 2003, 40:4-10.
5. Druker B.J., Tamura S., Buchdunger E., Ohno S., Segal G.M., Fanning S., et al. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med 1996, 2:561-566.
6. Baccarani M., Saglio G., Goldman J., Hochhaus A., Simonsson B., Appelbaum F., et al. Evolving concepts in the management of chronic myeloid leukemia: recommendations from an expert panel on behalf of the European LeukemiaNet. Blood 2006, 108:1809-1820.
7. Druker B.J., Talpaz M., Resta D.J., Peng B., Buchdunger E., Ford J.M., et al. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med 2001, 344:1031-1037.
8. Hochhaus A., Druker B., Sawyers C., Guilhot F., Schiffer C.A., Cortes J., et al. Favorable long-term follow-up results over 6 years for response, survival, and safety with imatinib mesylate therapy in chronic-phase chronic myeloid leukemia after failure of interferon-alpha treatment. Blood 2008, 111:1039-1043.
9. Hochhaus A., O'Brien S.G., Guilhot F., Druker B.J., Branford S., Foroni L., et al. Six-year follow-up of patients receiving imatinib for the first-line treatment of chronic myeloid leukemia. Leukemia 2009, 23:1054-1061.
10. Hochhaus A., Kreil S., Corbin A.S., La Rosee P., Muller M.C., Lahaye T., et al. Molecular and chromosomal mechanisms of resistance to imatinib (STI571) therapy. Leukemia 2002, 16:2190-2196.
11. Hochhaus A., La Rosee P. Imatinib therapy in chronic myelogenous leukemia: strategies to avoid and overcome resistance. Leukemia 2004, 18:1321-1331.
12. Apperley J.F. Part I: mechanisms of resistance to imatinib in chronic myeloid leukaemia. Lancet Oncol 2007, 8:1018-1029.
13. Cortes J.E., Talpaz M., Giles F., O'Brien S., Rios M.B., Shan J., et al. Prognostic significance of cytogenetic clonal evolution in patients with chronic myelogenous leukemia on imatinib mesylate therapy. Blood 2003, 101:3794-3800.
14. Weisberg E., Manley P.W., Breitenstein W., Bruggen J., Cowan-Jacob S.W., Ray A., et al. Characterization of AMN107, a selective inhibitor of native and mutant Bcr-Abl. Cancer Cell 2005, 7:129-141.
15. Shah N.P., Tran C., Lee F.Y., Chen P., Norris D., Sawyers C.L. Overriding imatinib resistance with a novel ABL kinase inhibitor. Science 2004, 305:399-401.
16. Kantarjian H., Giles F., Wunderle L., Bhalla K., O'Brien S., Wassmann B., et al. Nilotinib in imatinib-resistant CML and Philadelphia chromosome-positive ALL. N Engl J Med 2006, 354:2542-2551.
17. Talpaz M., Shah N.P., Kantarjian H., Donato N., Nicoll J., Paquette R., et al. Dasatinib in imatinib-resistant Philadelphia chromosome-positive leukemias. N Engl J Med 2006, 354:2531-2541.
18. Inoue K., Ogawa H., Yamagami T., Soma T., Tani Y., Tatekawa T., et al. Long-term follow-up of minimal residual disease in leukemia patients by monitoring WT1 (Wilms tumor gene) expression levels. Blood 1996, 88:2267-2278.
19. Martin H., Atta J., Bruecher J., Elsner S., Schardt C., Stadler M., et al. In patients with BCR-ABL-positive ALL in CR peripheral blood contains less residual disease than bone marrow: implications for autologous BMT. Ann Hematol 1994, 68:85-87.
20. Lord B.I., Testa N.G., Hendry J.H. The relative spatial distributions of CFUs and CFUc in the normal mouse femur. Blood 1975, 46:65-72.
21. Fliedner T.M., Graessle D., Paulsen C., Reimers K. Structure and function of bone marrow hemopoiesis: mechanisms of response to ionizing radiation exposure. Cancer Biother Radiopharm 2002, 17:405-426.
22. Tavassoli M. Structure and function of sinusoidal endothelium of bone marrow. Prog Clin Biol Res 1981, 59B:249-256.
23. Cipolleschi M.G., Dello Sbarba P., Olivotto M. The role of hypoxia in the maintenance of hematopoietic stem cells. Blood 1993, 82:2031-2037.
24. Scott L.M., Priestley G.V., Papayannopoulou T. Deletion of alpha4 integrins from adult hematopoietic cells reveals roles in homeostasis, regeneration, and homing. Mol Cell Biol 2003, 23:9349-9360.
25. Ulyanova T., Scott L.M., Priestley G.V., Jiang Y., Nakamoto B., Koni P.A., et al. VCAM-1 expression in adult hematopoietic and nonhematopoietic cells is controlled by tissue-inductive signals and reflects their developmental origin. Blood 2005, 106:86-94.
26. Broxmeyer H.E., Orschell C.M., Clapp D.W., Hangoc G., Cooper S., Plett P.A., et al. Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med 2005, 201:1307-1318.
27. Liles W.C., Broxmeyer H.E., Rodger E., Wood B., Hubel K., Cooper S., et al. Mobilization of hematopoietic progenitor cells in healthy volunteers by AMD3100, a CXCR4 antagonist. Blood 2003, 102:2728-2730.
28. Weiss R.A., Root W.S. Innervation of the vessels of the marrow cavity of certain bones. Am J Physiol 1959, 197:1255-1257.
29. Abkowitz J.L., Robinson A.E., Kale S., Long M.W., Chen J. Mobilization of hematopoietic stem cells during homeostasis and after cytokine exposure. Blood 2003, 102:1249-1253.
30. Wright D.E., Wagers A.J., Gulati A.P., Johnson F.L., Weissman I.L. Physiological migration of hematopoietic stem and progenitor cells. Science 2001, 294:1933-1936.
31. Schofield R. A comparative study of the repopulating potential of grafts from various haemopoietic sources: CFU repopulation. Cell Tissue Kinet 1970, 3:119-130.
32. Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 1978, 4:7-25.
33. Lo Celso C., Wu J.W., Lin C.P. In vivo imaging of hematopoietic stem cells and their microenvironment. J Biophotonics 2009, 2:619-631.
34. Nilsson S.K., Johnston H.M., Coverdale J.A. Spatial localization of transplanted hemopoietic stem cells: inferences for the localization of stem cell niches. Blood 2001, 97:2293-2299.
35. Calvi L.M., Adams G.B., Weibrecht K.W., Weber J.M., Olson D.P., Knight M.C., et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003, 425:841-846.
36. Kiel M.J., Radice G.L., Morrison S.J. Lack of evidence that hematopoietic stem cells depend on N-cadherin-mediated adhesion to osteoblasts for their maintenance. Cell Stem Cell 2007, 1:204-217.
37. Arai F., Hirao A., Ohmura M., Sato H., Matsuoka S., Takubo K., et al. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 2004, 118:149-161.
38. Zhang J., Niu C., Ye L., Huang H., He X., Tong W.G., et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003, 425:836-841.
39. Visnjic D., Kalajzic Z., Rowe D.W., Katavic V., Lorenzo J., Aguila H.L. Hematopoiesis is severely altered in mice with an induced osteoblast deficiency. Blood 2004, 103:3258-3264.
40. Adams G.B., Chabner K.T., Alley I.R., Olson D.P., Szczepiorkowski Z.M., Poznansky M.C., et al. Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor. Nature 2006, 439:599-603.
41. Nilsson S.K., Haylock D.N., Johnston H.M., Occhiodoro T., Brown T.J., Simmons P.J. Hyaluronan is synthesized by primitive hemopoietic cells, participates in their lodgment at the endosteum following transplantation, and is involved in the regulation of their proliferation and differentiation in vitro. Blood 2003, 101:856-862.
42. Semerad C.L., Christopher M.J., Liu F., Short B., Simmons P.J., Winkler I., et al. G-CSF potently inhibits osteoblast activity and CXCL12 mRNA expression in the bone marrow. Blood 2005, 106:3020-3027.
43. Stier S., Ko Y., Forkert R., Lutz C., Neuhaus T., Grunewald E., et al. Osteopontin is a hematopoietic stem cell niche component that negatively regulates stem cell pool size. J Exp Med 2005, 201:1781-1791.
44. Kiel M.J., Yilmaz O.H., Iwashita T., Yilmaz O.H., Terhorst C., Morrison S.J. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 2005, 121:1109-1121.
45. Engel P., Eck M.J., Terhorst C. The SAP and SLAM families in immune responses and X-linked lymphoproliferative disease. Nat Rev Immunol 2003, 3:813-821.
46. Sugiyama T., Kohara H., Noda M., Nagasawa T. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 2006, 25:977-988.
47. Parmar K., Mauch P., Vergilio J.A., Sackstein R., Down J.D. Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci USA 2007, 104:5431-5436.
48. Iwasaki H., Suda T. Cancer stem cells and their niche. Cancer Sci 2009, 100:1166-1172.
49. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003, 100:3983-3988.
50. Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997, 3:730-737.
51. Dalerba P., Dylla S.J., Park I.K., Liu R., Wang X., Cho R.W., et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA 2007, 104:10158-10163.
52. Li C., Heidt D.G., Dalerba P., Burant C.F., Zhang L., Adsay V., et al. Identification of pancreatic cancer stem cells. Cancer Res 2007, 67:1030-1037.
53. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., et al. Identification of human brain tumour initiating cells. Nature 2004, 432:396-401.
54. Wang J.C., Lapidot T., Cashman J.D., Doedens M., Addy L., Sutherland D.R., et al. High level engraftment of NOD/SCID mice by primitive normal and leukemic hematopoietic cells from patients with chronic myeloid leukemia in chronic phase. Blood 1998, 91:2406-2414.
55. Eaves C., Udomsakdi C., Cashman J., Barnett M., Eaves A. The biology of normal and neoplastic stem cells in CML. Leuk Lymphoma 1993, 11(Suppl. 1):245-253.
56. Hou L., Liu T., Tan J., Meng W., Deng L., Yu H., et al. Long-term culture of leukemic bone marrow primary cells in biomimetic osteoblast niche. Int J Hematol 2009.
57. Krause D.S., Lazarides K., von Andrian U.H., Van Etten R.A. Requirement for CD44 in homing and engraftment of BCR-ABL-expressing leukemic stem cells. Nat Med 2006, 12:1175-1180.
58. Valent P., Deininger M. Clinical perspectives of concepts on neoplastic stem cells and stem cell-resistance in chronic myeloid leukemia. Leuk Lymphoma 2008, 49:604-609.
59. Graham S.M., Jorgensen H.G., Allan E., Pearson C., Alcorn M.J., Richmond L., et al. Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. Blood 2002, 99:319-325.
60. Brendel C., Scharenberg C., Dohse M., Robey R.W., Bates S.E., Shukla S., et al. Imatinib mesylate and nilotinib (AMN107) exhibit high-affinity interaction with ABCG2 on primitive hematopoietic stem cells. Leukemia 2007, 21:1267-1275.
61. Jiang X., Zhao Y., Smith C., Gasparetto M., Turhan A., Eaves A., et al. Chronic myeloid leukemia stem cells possess multiple unique features of resistance to BCR-ABL targeted therapies. Leukemia 2007, 21:926-935.
62. Wang L., Giannoudis A., Lane S., Williamson P., Pirmohamed M., Clark R.E. Expression of the uptake drug transporter hOCT1 is an important clinical determinant of the response to imatinib in chronic myeloid leukemia. Clin Pharmacol Ther 2008, 83:258-264.
63. Sorel N., Bonnet M.L., Guillier M., Guilhot F., Brizard A., Turhan A.G. Evidence of ABL-kinase domain mutations in highly purified primitive stem cell populations of patients with chronic myelogenous leukemia. Biochem Biophys Res Commun 2004, 323:728-730.
64. Roche-Lestienne C., Preudhomme C. Mutations in the ABL kinase domain pre-exist the onset of imatinib treatment. Semin Hematol 2003, 40:80-82.
65. Chu S., Xu H., Shah N.P., Snyder D.S., Forman S.J., Sawyers C.L., et al. Detection of BCR-ABL kinase mutations in CD34+ cells from chronic myelogenous leukemia patients in complete cytogenetic remission on imatinib mesylate treatment. Blood 2005, 105:2093-2098.
66. Copland M., Hamilton A., Elrick L.J., Baird J.W., Allan E.K., Jordanides N., et al. Dasatinib (BMS-354825) targets an earlier progenitor population than imatinib in primary CML but does not eliminate the quiescent fraction. Blood 2006, 107:4532-4539.
67. Jamieson C.H. Chronic myeloid leukemia stem cells. Hematol Am Soc Hematol Educ Program 2008, 436-442.
68. Reya T., Duncan A.W., Ailles L., Domen J., Scherer D.C., Willert K., et al. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 2003, 423:409-414.
69. Stein M.I., Zhu J., Emerson S.G. Molecular pathways regulating the self-renewal of hematopoietic stem cells. Exp Hematol 2004, 32:1129-1136.
70. Jamieson C.H., Ailles L.E., Dylla S.J., Muijtjens M., Jones C., Zehnder J.L., et al. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med 2004, 351:657-667.
71. Sengupta A., Banerjee D., Chandra S., Banerji S.K., Ghosh R., Roy R., et al. Deregulation and cross talk among Sonic hedgehog, Wnt, Hox and Notch signaling in chronic myeloid leukemia progression. Leukemia 2007, 21:949-955.
72. Ito K., Bernardi R., Morotti A., Matsuoka S., Saglio G., Ikeda Y., et al. PML targeting eradicates quiescent leukaemia-initiating cells. Nature 2008, 453:1072-1078.
73. Holtz M.S., Forman S.J., Bhatia R. Nonproliferating CML CD34+ progenitors are resistant to apoptosis induced by a wide range of proapoptotic stimuli. Leukemia 2005, 19:1034-1041.
74. Molofsky A.V., Pardal R., Iwashita T., Park I.K., Clarke M.F., Morrison S.J. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 2003, 425:962-967.
75. Park I.K., Qian D., Kiel M., Becker M.W., Pihalja M., Weissman I.L., et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 2003, 423:302-305.
76. Giafis N., Katsoulidis E., Sassano A., Tallman M.S., Higgins L.S., Nebreda A.R., et al. Role of the p38 mitogen-activated protein kinase pathway in the generation of arsenic trioxide-dependent cellular responses. Cancer Res 2006, 66:6763-6771.
77. Ito K., Hirao A., Arai F., Takubo K., Matsuoka S., Miyamoto K., et al. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat Med 2006, 12:446-451.
78. Florian S., Sonneck K., Hauswirth A.W., Krauth M.T., Schernthaner G.H., Sperr W.R., et al. Detection of molecular targets on the surface of CD34+/CD38- stem cells in various myeloid malignancies. Leuk Lymphoma 2006, 47:207-222.
79. Dierks C., Beigi R., Guo G.R., Zirlik K., Stegert M.R., Manley P., et al. Expansion of Bcr-Abl-positive leukemic stem cells is dependent on Hedgehog pathway activation. Cancer Cell 2008, 14:238-249.
80. Chu S., Holtz M., Gupta M., Bhatia R. BCR/ABL kinase inhibition by imatinib mesylate enhances MAP kinase activity in chronic myelogenous leukemia CD34+ cells. Blood 2004, 103:3167-3174.
81. Deacon K., Mistry P., Chernoff J., Blank J.L., Patel R. p38 Mitogen-activated protein kinase mediates cell death and p21-activated kinase mediates cell survival during chemotherapeutic drug-induced mitotic arrest. Mol Biol Cell 2003, 14:2071-2087.
82. Kantarjian H.M., Larson R.A., Guilhot F., O'Brien S.G., Mone M., Rudoltz M., et al. Efficacy of imatinib dose escalation in patients with chronic myeloid leukemia in chronic phase. Cancer 2009, 115:551-560.
83. Cortes J.E., Baccarani M., Guilhot F., Druker B.J., Branford S., Kim D.W., et al. Phase III, randomized, open-label study of daily imatinib mesylate 400mg versus 800mg in patients with newly diagnosed, previously untreated chronic myeloid leukemia in chronic phase using molecular end points: tyrosine kinase inhibitor optimization and selectivity study. J Clin Oncol 2010, 28:424-430.
84. Golemovic M., Verstovsek S., Giles F., Cortes J., Manshouri T., Manley P.W., et al. AMN107, a novel aminopyrimidine inhibitor of Bcr-Abl, has in vitro activity against imatinib-resistant chronic myeloid leukemia. Clin Cancer Res 2005, 11:4941-4947.
85. Lombardo L.J., Lee F.Y., Chen P., Norris D., Barrish J.C., Behnia K., et al. Discovery of N-(2-chloro-6-methyl-phenyl)-2-(6-(4-(2-hydroxyethyl)-piperazin-1-yl)-2-methylpyrimidin-4-ylamino)thiazole-5-carboxamide (BMS-354825), a dual Src/Abl kinase inhibitor with potent antitumor activity in preclinical assays. J Med Chem 2004, 47:6658-6661.
86. Jabbour E., Kantarjian H., Jones D., Talpaz M., Bekele N., O'Brien S., et al. Frequency and clinical significance of BCR-ABL mutations in patients with chronic myeloid leukemia treated with imatinib mesylate. Leukemia 2006, 20:1767-1773.
87. Branford S., Rudzki Z., Walsh S., Parkinson I., Grigg A., Szer J., et al. Detection of BCR-ABL mutations in patients with CML treated with imatinib is virtually always accompanied by clinical resistance, and mutations in the ATP phosphate-binding loop (P-loop) are associated with a poor prognosis. Blood 2003, 102:276-283.
88. Hughes T., Deininger M., Hochhaus A., Branford S., Radich J., Kaeda J., et al. Monitoring CML patients responding to treatment with tyrosine kinase inhibitors: review and recommendations for harmonizing current methodology for detecting BCR-ABL transcripts and kinase domain mutations and for expressing results. Blood 2006, 108:28-37.
89. Jabbour E., Kantarjian H.M., Jones D., Reddy N., O'Brien S., Garcia-Manero G., et al. Characteristics and outcome of chronic myeloid leukemia patients with F317L BCR-ABL kinase domain mutation after therapy with tyrosine kinase inhibitors. Blood 2008, 112:4839-4842.
90. Soverini S., Colarossi S., Gnani A., Rosti G., Castagnetti F., Poerio A., et al. Contribution of ABL kinase domain mutations to imatinib resistance in different subsets of Philadelphia-positive patients: by the GIMEMA Working Party on Chronic Myeloid Leukemia. Clin Cancer Res 2006, 12:7374-7379.
91. Giles F.J., Cortes J., Jones D., Bergstrom D., Kantarjian H., Freedman S.J. MK-0457, a novel kinase inhibitor, is active in patients with chronic myeloid leukemia or acute lymphocytic leukemia with the T315I BCR-ABL mutation. Blood 2007, 109:500-502.
92. Gontarewicz A., Balabanov S., Keller G., Colombo R., Graziano A., Pesenti E., et al. Simultaneous targeting of Aurora kinases and Bcr-Abl kinase by the small molecule inhibitor PHA-739358 is effective against imatinib-resistant BCR-ABL mutations including T315I. Blood 2008, 111:4355-4364.
93. Seeliger M.A., Ranjitkar P., Kasap C., Shan Y., Shaw D.E., Shah N.P., et al. Equally potent inhibition of c-Src and Abl by compounds that recognize inactive kinase conformations. Cancer Res 2009, 69:2384-2392.
94. Pinilla-Ibarz J., Quintas-Cardama A. New agents in the treatment of chronic myelogenous leukemia. J Natl Compr Canc Netw 2009, 7:1028-1037.
95. Zhang J., Adrian F.J., Jahnke W., Cowan-Jacob S.W., Li A.G., Iacob R.E., et al. Targeting Bcr-Abl by combining allosteric with ATP-binding-site inhibitors. Nature 2010, 463:501-506.
96. Illmer T., Schaich M., Platzbecker U., Freiberg-Richter J., Oelschlagel U., von Bonin M., et al. P-glycoprotein-mediated drug efflux is a resistance mechanism of chronic myelogenous leukemia cells to treatment with imatinib mesylate. Leukemia 2004, 18:401-408.
97. Thomas J., Wang L., Clark R.E., Pirmohamed M. Active transport of imatinib into and out of cells: implications for drug resistance. Blood 2004, 104:3739-3745.
98. Hiwase D.K., Saunders V., Hewett D., Frede A., Zrim S., Dang P., et al. Dasatinib cellular uptake and efflux in chronic myeloid leukemia cells: therapeutic implications. Clin Cancer Res 2008, 14:3881-3888.
99. White D.L., Saunders V.A., Dang P., Engler J., Zannettino A.C., Cambareri A.C., et al. 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 2006, 108:697-704.
100. Angstreich G.R., Matsui W., Huff C.A., Vala M.S., Barber J., Hawkins A.L., et al. Effects of imatinib and interferon on primitive chronic myeloid leukaemia progenitors. Br J Haematol 2005, 130:373-381.
101. Talpaz M., Estrov Z., Kantarjian H., Ku S., Foteh A., Kurzrock R. Persistence of dormant leukemic progenitors during interferon-induced remission in chronic myelogenous leukemia. Analysis by polymerase chain reaction of individual colonies. J Clin Invest 1994, 94:1383-1389.
102. Rousselot P., Huguet F., Rea D., Legros L., Cayuela J.M., Maarek O., et al. Imatinib mesylate discontinuation in patients with chronic myelogenous leukemia in complete molecular remission for more than 2 years. Blood 2007, 109:58-60.
103. Gratwohl A., Heim D. Current role of stem cell transplantation in chronic myeloid leukaemia. Best Pract Res Clin Haematol 2009, 22:431-443.
104. Clark B.R., Keating A. Biology of bone marrow stroma. Ann N Y Acad Sci 1995, 770:70-78.
105. Verfaillie C., Hurley R., Bhatia R., McCarthy J.B. Role of bone marrow matrix in normal and abnormal hematopoiesis. Crit Rev Oncol Hematol 1994, 16:201-224.
106. Dazzi F., Ramasamy R., Glennie S., Jones S.P., Roberts I. The role of mesenchymal stem cells in haemopoiesis. Blood Rev 2006, 20:161-171.
107. Friedenstein A.J., Deriglasova U.F., Kulagina N.N., Panasuk A.F., Rudakowa S.F., Luria E.A., et al. Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp Hematol 1974, 2:83-92.
108. Al-Khaldi A., Eliopoulos N., Martineau D., Lejeune L., Lachapelle K., Galipeau J. Postnatal bone marrow stromal cells elicit a potent VEGF-dependent neoangiogenic response in vivo. Gene Ther 2003, 10:621-629.
109. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147.
110. Reyes M., Lund T., Lenvik T., Aguiar D., Koodie L., Verfaillie C.M. Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood 2001, 98:2615-2625.
111. Horwitz E.M., Le Blanc K., Dominici M., Mueller I., Slaper-Cortenbach I., Marini F.C., et al. Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy 2005, 7:393-395.
112. Kemp K.C., Hows J., Donaldson C. Bone marrow-derived mesenchymal stem cells. Leuk Lymphoma 2005, 46:1531-1544.
113. Roorda B.D., ter Elst A., Kamps W.A., de Bont E.S. Bone marrow-derived cells and tumor growth: contribution of bone marrow-derived cells to tumor micro-environments with special focus on mesenchymal stem cells. Crit Rev Oncol Hematol 2009, 69:187-198.
114. Nakashima K., de Crombrugghe B. Transcriptional mechanisms in osteoblast differentiation and bone formation. Trends Genet 2003, 19:458-466.
115. Rosen E.D., Walkey C.J., Puigserver P., Spiegelman B.M. Transcriptional regulation of adipogenesis. Genes Dev 2000, 14:1293-1307.
116. Hong J.H., Hwang E.S., McManus M.T., Amsterdam A., Tian Y., Kalmukova R., et al. TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science 2005, 309:1074-1078.
117. Majumdar M.K., Thiede M.A., Haynesworth S.E., Bruder S.P., Gerson S.L. Human marrow-derived mesenchymal stem cells (MSCs) express hematopoietic cytokines and support long-term hematopoiesis when differentiated toward stromal and osteogenic lineages. J Hematother Stem Cell Res 2000, 9:841-848.
118. Majumdar M.K., Thiede M.A., Mosca J.D., Moorman M., Gerson S.L. Phenotypic and functional comparison of cultures of marrow-derived mesenchymal stem cells (MSCs) and stromal cells. J Cell Physiol 1998, 176:57-66.
119. Baggiolini M. Chemokines and leukocyte traffic. Nature 1998, 392:565-568.
120. Deans R.J., Moseley A.B. Mesenchymal stem cells: biology and potential clinical uses. Exp Hematol 2000, 28:875-884.
121. Torlakovic E., Tenstad E., Funderud S., Rian E. CD10+ stromal cells form B-lymphocyte maturation niches in the human bone marrow. J Pathol 2005, 205:311-317.
122. Milne C.D., Fleming H.E., Zhang Y., Paige C.J. Mechanisms of selection mediated by interleukin-7, the preBCR, and hemokinin-1 during B-cell development. Immunol Rev 2004, 197:75-88.
123. Barda-Saad M., Rozenszajn L.A., Globerson A., Zhang A.S., Zipori D. Selective adhesion of immature thymocytes to bone marrow stromal cells: relevance to T cell lymphopoiesis. Exp Hematol 1996, 24:386-391.
124. Mazo I.B., Honczarenko M., Leung H., Cavanagh L.L., Bonasio R., Weninger W., et al. Bone marrow is a major reservoir and site of recruitment for central memory CD8+ T cells. Immunity 2005, 22:259-270.
125. Le Blanc K., Tammik C., Rosendahl K., Zetterberg E., Ringden O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol 2003, 31:890-896.
126. Tse W.T., Pendleton J.D., Beyer W.M., Egalka M.C., Guinan E.C. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 2003, 75:389-397.
127. Di Nicola M., Carlo-Stella C., Magni M., Milanesi M., Longoni P.D., Matteucci P., et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002, 99:3838-3843.
128. Krampera M., Glennie S., Dyson J., Scott D., Laylor R., Simpson E., et al. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood 2003, 101:3722-3729.
129. Djouad F., Plence P., Bony C., Tropel P., Apparailly F., Sany J., et al. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 2003, 102:3837-3844.
130. Le Blanc K., Rasmusson I., Sundberg B., Gotherstrom C., Hassan M., Uzunel M., et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 2004, 363:1439-1441.
131. Aggarwal S., Pittenger M.F. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005, 105:1815-1822.
132. Beyth S., Borovsky Z., Mevorach D., Liebergall M., Gazit Z., Aslan H., et al. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood 2005, 105:2214-2219.
133. Marastoni S., Ligresti G., Lorenzon E., Colombatti A., Mongiat M. Extracellular matrix: a matter of life and death. Connect Tissue Res 2008, 49:203-206.
134. Gilmore A.P. Anoikis. Cell Death Differ 2005, 12(Suppl. 2):1473-1477.
135. Hynes R.O. Integrins: a family of cell surface receptors. Cell 1987, 48:549-554.
136. Zhu J., Carman C.V., Kim M., Shimaoka M., Springer T.A., Luo B.H. Requirement of alpha and beta subunit transmembrane helix separation for integrin outside-in signaling. Blood 2007, 110:2475-2483.
137. Luo B.H., Carman C.V., Springer T.A. Structural basis of integrin regulation and signaling. Annu Rev Immunol 2007, 25:619-647.
138. Paget S. The distribution of secondary growths in cancer of the breast. 1889. Cancer Metastasis Rev 1989, 8:98-101.
139. Bhatia R., McGlave P.B., Dewald G.W., Blazar B.R., Verfaillie C.M. Abnormal function of the bone marrow microenvironment in chronic myelogenous leukemia: role of malignant stromal macrophages. Blood 1995, 85:3636-3645.
140. Colmone A., Amorim M., Pontier A.L., Wang S., Jablonski E., Sipkins D.A. Leukemic cells create bone marrow niches that disrupt the behavior of normal hematopoietic progenitor cells. Science 2008, 322:1861-1865.
141. Oberlin E., Amara A., Bachelerie F., Bessia C., Virelizier J.L., Arenzana-Seisdedos F., et al. The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1. Nature 1996, 382:833-835.
142. Peled A., Petit I., Kollet O., Magid M., Ponomaryov T., Byk T., et al. Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 1999, 283:845-848.
143. Vianello F., Villanova F., Tisato V., Lymperi S., Ho K.K., Gomes A.R., et al. Bone marrow mesenchymal stromal cells non-selectively protect chronic myeloid leukemia cells from imatinib-induced apoptosis via the CXCR4/CXCL12 axis. Haematologica 2010.
144. Williams R.T., den Besten W., Sherr C.J. Cytokine-dependent imatinib resistance in mouse BCR-ABL+Arf-null lymphoblastic leukemia. Genes Dev 2007, 21:2283-2287.
145. Bewry N.N., Nair R.R., Emmons M.F., Boulware D., Pinilla-Ibarz J., Hazlehurst L.A. Stat3 contributes to resistance toward BCR-ABL inhibitors in a bone marrow microenvironment model of drug resistance. Mol Cancer Ther 2008, 7:3169-3175.
146. Wang Y., Cai D., Brendel C., Barett C., Erben P., Manley P.W., et al. 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 2007, 109:2147-2155.
147. Damiano J.S., Cress A.E., Hazlehurst L.A., Shtil A.A., Dalton W.S. Cell adhesion mediated drug resistance (CAM-DR): role of integrins and resistance to apoptosis in human myeloma cell lines. Blood 1999, 93:1658-1667.
148. Damiano J.S., Dalton W.S. Integrin-mediated drug resistance in multiple myeloma. Leuk Lymphoma 2000, 38:71-81.
149. Sethi T., Rintoul R.C., Moore S.M., MacKinnon A.C., Salter D., Choo C., et al. Extracellular matrix proteins protect small cell lung cancer cells against apoptosis: a mechanism for small cell lung cancer growth and drug resistance in vivo. Nat Med 1999, 5:662-668.
150. Damiano J.S., Hazlehurst L.A., Dalton W.S. Cell adhesion-mediated drug resistance (CAM-DR) protects the K562 chronic myelogenous leukemia cell line from apoptosis induced by BCR/ABL inhibition, cytotoxic drugs, and gamma-irradiation. Leukemia 2001, 15:1232-1239.
151. Lundell B.I., McCarthy J.B., Kovach N.L., Verfaillie C.M. Activation-dependent alpha5beta1 integrin-mediated adhesion to fibronectin decreases proliferation of chronic myelogenous leukemia progenitors and K562 cells. Blood 1996, 87:2450-2458.
152. Hazlehurst L.A., Argilagos R.F., Dalton W.S. Beta1 integrin mediated adhesion increases Bim protein degradation and contributes to drug resistance in leukaemia cells. Br J Haematol 2007, 136:269-275.
153. Luciano F., Jacquel A., Colosetti P., Herrant M., Cagnol S., Pages G., et al. Phosphorylation of Bim-EL by Erk1/2 on serine 69 promotes its degradation via the proteasome pathway and regulates its proapoptotic function. Oncogene 2003, 22:6785-6793.
154. Kuribara R., Honda H., Matsui H., Shinjyo T., Inukai T., Sugita K., et al. Roles of Bim in apoptosis of normal and Bcr-Abl-expressing hematopoietic progenitors. Mol Cell Biol 2004, 24:6172-6183.
155. Burchert A., Wang Y., Cai D., von Bubnoff N., Paschka P., Muller-Brusselbach S., et al. Compensatory PI3-kinase/Akt/mTor activation regulates imatinib resistance development. Leukemia 2005, 19:1774-1782.
156. Mayerhofer M., Valent P., Sperr W.R., Griffin J.D., Sillaber C. BCR/ABL induces expression of vascular endothelial growth factor and its transcriptional activator, hypoxia inducible factor-1alpha, through a pathway involving phosphoinositide 3-kinase and the mammalian target of rapamycin. Blood 2002, 100:3767-3775.
157. Dengler J., von Bubnoff N., Decker T., Peschel C., Duyster J. Combination of imatinib with rapamycin or RAD001 acts synergistically only in Bcr-Abl-positive cells with moderate resistance to imatinib. Leukemia 2005, 19:1835-1838.
158. Cortes J., Albitar M., Thomas D., Giles F., Kurzrock R., Thibault A., et al. Efficacy of the farnesyl transferase inhibitor R115777 in chronic myeloid leukemia and other hematologic malignancies. Blood 2003, 101:1692-1697.
159. Cortes J., Quintas-Cardama A., Garcia-Manero G., O'Brien S., Jones D., Faderl S., et al. Phase 1 study of tipifarnib in combination with imatinib for patients with chronic myelogenous leukemia in chronic phase after imatinib failure. Cancer 2007, 110:2000-2006.
160. Peters D.G., Hoover R.R., Gerlach M.J., Koh E.Y., Zhang H., Choe K., et al. Activity of the farnesyl protein transferase inhibitor SCH66336 against BCR/ABL-induced murine leukemia and primary cells from patients with chronic myeloid leukemia. Blood 2001, 97:1404-1412.
161. Yu C., Krystal G., Varticovksi L., McKinstry R., Rahmani M., Dent P., et al. Pharmacologic mitogen-activated protein/extracellular signal-regulated kinase kinase/mitogen-activated protein kinase inhibitors interact synergistically with STI571 to induce apoptosis in Bcr/Abl-expressing human leukemia cells. Cancer Res 2002, 62:188-199.
162. Nguyen T.K., Rahmani M., Harada H., Dent P., Grant S. MEK1/2 inhibitors sensitize Bcr/Abl+ human leukemia cells to the dual Abl/Src inhibitor BMS-354/825. Blood 2007, 109:4006-4015.
163. Nimmanapalli R., O'Bryan E., Bhalla K. Geldanamycin and its analogue 17-allylamino-17-demethoxygeldanamycin lowers Bcr-Abl levels and induces apoptosis and differentiation of Bcr-Abl-positive human leukemic blasts. Cancer Res 2001, 61:1799-1804.
164. Radujkovic A., Schad M., Topaly J., Veldwijk M.R., Laufs S., Schultheis B.S., et al. Synergistic activity of imatinib and 17-AAG in imatinib-resistant CML cells overexpressing BCR-ABL-inhibition of P-glycoprotein function by 17-AAG. Leukemia 2005, 19:1198-1206.
165. Gatto S., Scappini B., Pham L., Onida F., Milella M., Ball G., et al. The proteasome inhibitor PS-341 inhibits growth and induces apoptosis in Bcr/Abl-positive cell lines sensitive and resistant to imatinib mesylate. Haematologica 2003, 88:853-863.
166. Nimmanapalli R., Fuino L., Stobaugh C., Richon V., Bhalla K. Cotreatment with the histone deacetylase inhibitor suberoylanilide hydroxamic acid (SAHA) enhances imatinib-induced apoptosis of Bcr-Abl-positive human acute leukemia cells. Blood 2003, 101:3236-3239.
167. Yu C., Rahmani M., Almenara J., Subler M., Krystal G., Conrad D., et al. Histone deacetylase inhibitors promote STI571-mediated apoptosis in STI571-sensitive and -resistant Bcr/Abl+ human myeloid leukemia cells. Cancer Res 2003, 63:2118-2126.
168. Yu C., Krystal G., Dent P., Grant S. Flavopiridol potentiates STI571-induced mitochondrial damage and apoptosis in BCR-ABL-positive human leukemia cells. Clin Cancer Res 2002, 8:2976-2984.
169. Fiskus W., Pranpat M., Bali P., Balasis M., Kumaraswamy S., Boyapalle S., et al. Combined effects of novel tyrosine kinase inhibitor AMN107 and histone deacetylase inhibitor LBH589 against Bcr-Abl-expressing human leukemia cells. Blood 2006, 108:645-652.
170. Morotti A., Cilloni D., Messa F., Arruga F., Defilippi I., Carturan S., et al. Valproate enhances imatinib-induced growth arrest and apoptosis in chronic myeloid leukemia cells. Cancer 2006, 106:1188-1196.
171. Dillmann F., Veldwijk M.R., Laufs S., Sperandio M., Calandra G., Wenz F., et al. Plerixafor inhibits chemotaxis toward SDF-1 and CXCR4-mediated stroma contact in a dose-dependent manner resulting in increased susceptibility of BCR-ABL+ cell to Imatinib and Nilotinib. Leuk Lymphoma 2009, 50:1676-1686.
172. Jiang X., Lopez A., Holyoake T., Eaves A., Eaves C. Autocrine production and action of IL-3 and granulocyte colony-stimulating factor in chronic myeloid leukemia. Proc Natl Acad Sci USA 1999, 96:12804-12809.
173. Zhang X., Ren R. 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 1998, 92:3829-3840.
174. Weitz-Schmidt G., Welzenbach K., Brinkmann V., Kamata T., Kallen J., Bruns C., et al. Statins selectively inhibit leukocyte function antigen-1 by binding to a novel regulatory integrin site. Nat Med 2001, 7:687-692.