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Kinase-inhibitor–insensitive cancer stem cells in chronic myeloid leukemia

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Bibliography

  • Nowell PC. Discovery of the Philadelphia chromosome: a personal perspective. J Clin Invest 2007;117:2033-5
  • Druker BJ. Translation of the Philadelphia chromosome into therapy for CML. Blood 2008;112:4808-17
  • Melo JV, Barnes DJ. Chronic myeloid leukaemia as a model of disease evolution in human cancer. Nat Rev Cancer 2007;7:441-53
  • Ren R. Mechanisms of BCR-ABL in the pathogenesis of chronic myelogenous leukaemia. Nat Rev Cancer 2005;5:172-83
  • Pear WS, Miller JP, Xu L, et al. Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving p210 bcr/abl-transduced bone marrow. Blood 1998;92:3780-92
  • Wong S, Witte ON. Modeling Philadelphia chromosome positive leukemias. Oncogene 2001;20:5644-59
  • Deininger M, Buchdunger E, Druker BJ. The development of imatinib as a therapeutic agent for chronic myeloid leukemia. Blood 2005;105:2640-53
  • Kantarjian HM, Shah NP, Cortes JE, et al. Dasatinib or imatinib in newly diagnosed chronic-phase chronic myeloid leukemia: 2-year follow-up from a randomized phase 3 trial (DASISION). Blood 2012;119:1123-9
  • Larson RA, Hochhaus A, Hughes TP, et al. Nilotinib vs imatinib in patients with newly diagnosed Philadelphia chromosome-positive chronic myeloid leukemia in chronic phase: ENESTnd 3-year follow-up. Leukemia 2012;26:2197-203
  • Branford S, Kim DW, Soverini S, et al. Initial molecular response at 3 months may predict both response and event-free survival at 24 months in imatinib-resistant or -intolerant patients with Philadelphia chromosome-positive chronic myeloid leukemia in chronic phase treated with nilotinib. J Clin Oncol 2012;30:4323-9
  • Jabbour E, Saglio G, Hughes TP, et al. Suboptimal responses in chronic myeloid leukemia: implications and management strategies. Cancer 2012;118:1181-91
  • Baccarani M, Deininger MW, Rosti G, et al. European LeukemiaNet recommendations for the management of chronic myeloid leukemia: 2013. Blood 2013;122:872-84
  • Cross NC, White HE, Müller MC, et al. Standardized definitions of molecular response in chronic myeloid leukemia. Leukemia 2012;26:2172-5
  • Weisberg E, Manley PW, Cowan-Jacob SW, et al. Second generation inhibitors of BCRABL for the treatment of imatinib resistant chronic myeloid leukaemia. Nat Rev Cancer 2007;7:345-56
  • Saglio G, Kim DW, Issaragrisil S, et al. Nilotinib versus imatinib for newly diagnosed chronic myeloid leukemia. N Engl J Med 2010;17:2251-9
  • Mahon FX, Réa D, Guilhot J, et al. Discontinuation of imatinib in patients with chronic myeloid leukaemia who have maintained complete molecular remission for at least 2 years: the prospective, multicentre Stop Imatinib (STIM) trial. Lancet Oncol 2010;11:1029-35
  • Nardi V, Azam M, Daley GQ. Mechanisms and implications of imatinib resistance mutations in BCR-ABL. Curr Opin Hematol 2004;11:35-43
  • Graham SM, Jørgensen HG, Allan E, et al. Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. Blood 2002;99:319-25
  • Jiang X, Forrest D, Nicolini F, et al. Properties of CD34 CMLstem/progenitor cells that correlate with different clinical responses to imatinib mesylate. Blood 2010;116:2112-21
  • Copland M, Hamilton A, Elrick LJ, et al. Dasatinib (BMS-354825) targets an earlier progenitor population than imatinib in primary CML but does not eliminate the quiescent fraction. Blood 2006;107:4532-9
  • Jørgensen HG, Allan EK, Jordanides NE, et al. Nilotinib exerts equipotent antiproliferative effects to imatinib and does not induce apoptosis in CD34+ CML cells. Blood 2007;109:4016-19
  • Konig H, Holtz M, Modi H, et al. Enhanced BCR-ABL kinase inhibition does not result in increased inhibition of downstream signaling pathways or increased growth suppression in CML progenitors. Leukemia 2008;22:748-55
  • Savona M, Talpaz M. Getting to the stem of chronic myeloid leukaemia. Nat Rev Cancer 2008;8:341-50
  • Elrick LJ, Jorgensen HG, Mountford JC, et al. Punish the parent not the progeny. Blood 2005;105(5):1862-6
  • Perl A, Carroll M. BCR-ABL kinase is dead; long live the CML stem cell. J Clin Invest 2011;121:22-5
  • Corbin AS, Agarwal A, Loriaux M, et al. Human chronic myeloid leukemia stem cells are insensitive to imatinib despite inhibition of BCR-ABL activity. J Clin Invest 2011;121:396-409
  • Jordanides NE, Jorgensen HG, Holyoake TL, et al. FunctionalABCG2 is overexpressed on primary CML CD34 cells and is inhibited by imatinib mesylate. Blood 2006;108:1370-3
  • Hatziieremia S, Jordanides NE, Holyoake TL, et al. Inhibition of MDR1 does not sensitize primitive chronic myeloid leukemia CD34+ cells to imatinib. Exp Hematol 2009;37:692-700
  • Davies A, Jordanides NE, Giannoudis A, et al. Nilotinib concentration in cell lines and primary CD34(+) chronic myeloid leukemia cells is not mediated by active uptake or efflux by major drug transporters. Leukemia 2009;23:1999-2006
  • Hamilton A, Helgason GV, Schemionek M, et al. Chronic myeloid leukemia stem cells are not dependent on Bcr-Abl kinase activity for their survival. Blood 2012;119:1501-10
  • Bernardi R, Pandolfi PP. Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat Rev Cancer 2007;8:1006-16
  • Reineke EL, Kao HY. PML: an emerging tumor suppressor and a target with therapeutic potential. Cancer Ther 2009;7:219-26
  • Ito K, Bernardi R, Pandolfi PP. A novel signaling network as a critical rheostat for the biology and maintenance of the normal stem cell and the cancer-initiating cell. Curr Opin Genet Dev 2009;19:51-9
  • Ito K, Bernardi R, Morotti A, et al. PML targeting eradicates quiescent leukaemia-initiating cells. Nature 2008;453:1072-8
  • Kashimura M, Ohyashiki K. Successful imatinib and arsenic trioxide combination therapy for sudden onset promyelocytic crisis with t(15;17) in chronic myeloid leukemia. Leuk Res 2010;34:e213-14
  • Burgering BM. A brief introduction to FOXOlogy. Oncogene 2008;27:2258-62
  • Lam EW, Brosens JJ, Gomes AR, et al. Forkhead box proteins: tuning forks for transcriptional harmony. Nat Rev Cancer 2013;13:482-95
  • Tothova Z, Kollipara R, Huntly BJ, et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 2007;128:325-39
  • Naka K, Hoshii T, Muraguchi T, et al. TGF-beta-FOXO signaling maintains leukaemia-initiating cells in chronic myeloid leukemia. Nature 2010;463:676-8
  • Duy C, Hurtz C, Shojaee S, et al. BCL6 enables Ph+ acute lymphoblastic leukaemia cells to survive BCR-ABL1 kinase inhibition. Nature 2011;473:384-8
  • Hurtz C, Hatzi K, Cerchietti L, et al. BCL6-mediated repression of p53 is critical for leukemia stem cell survival in chronic myeloid leukemia. J Exp Med 2011;208:2163-74
  • Dierks C, Beigi R, Guo GR, et al. Expansion of Bcr-Abl-positive leukemic stem cells is dependent on Hedgehog pathway activation. Cancer Cell 2008;14:238-49
  • Long B, Zhu H, Zhu C, et al. Activation of the hedgehog pathway in chronic myelogeneous leukemia patients. J Exp Clin Cancer Res 2011;30:1-5
  • Zhao C, Chen A, Jamieson CH, et al. Hedgehog signaling is essential for maintenance of cancer stem cells in myeloid leukaemia. Nature 2009;458:776-80
  • Kawaguchi-Ihara N, Okuhashi Y, Itoh M, et al. Promotion of the self-renewal capacity of human leukemia cells by sonic hedgehog protein. Anticancer Res 2011;31:781-4
  • Cao L, Bombard J, Cintron K, et al. BMI1 as a novel target for drug discovery in cancer. J Cell Biochem 2011;112:2729-41
  • Grinstein E, Mahotka C. Stem cell divisions controlled by the proto-oncogene BMI-1. J Stem Cells 2009;4:141-6
  • Raaphorst FM. Self-renewal of hematopoietic and leukemic stem cells: a central role for the Polycomb-group gene Bmi-1. Trends Immunol 2003;2410:522-4
  • Iwama A, Oguro H, Negishi M, et al. Enhanced self renewal of hematopoietic stem cells mediated by the polycomb gene product Bmi-1. Immunity 2004;21:843-51
  • Park IK, Qian D, Kiel M, et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 2003;423:302-5
  • Lessard J, Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 2003;423:255-60
  • Minucci S, Pelicci PG. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer 2006;6:38-51
  • Yu C, Rahmani M, Almenara J, et al. Histone deacetylase inhibitors promote STI571-mediated apoptosis in STI571-sensitive and -resistant Bcr/Abl human myeloid leukemia cells. Cancer Res 2003;63:2118-26
  • Nimmanapalli R, Fuino L, Bali P, et al. Histone deacetylase inhibitor LAQ824 both lowers expression and promotes proteasomal degradation of Bcr-Abl and induces apoptosis of imatinib mesylate-sensitive or -refractory chronic myelogenous leukemia-blast crisis cells. Cancer Res 2003;63:5126-35
  • Nimmanapalli R, Fuino L, Stobaugh C, et al. Cotreatment with the histone deacteylase inhibitor suberoylanilide hydroxamic acid (SAHA) enhances imatinib-induced apoptosis of Bcr-Abl-positive human acute leukemia cells. Blood 2003;101:3236-9
  • Rosato RR, Almenara JA, Grant S. The histone deacetylase inhibitor MS-275 promotes differentiation or apoptosis in human leukemia cells through a process regulated by generation of reactive oxygen species and induction of p21CIP/WAF1. Cancer Res 2003;63:3637-45
  • Morotti A, Cilloni D, Messa F, et al. Valproate enhances imatinib-induced growth arrest and apoptosis in chronic myeloid leukemia cells. Cancer 2006;106:1188-96
  • Zhang B, Strauss AC, Chu S, et al. Effective targeting of quiescent chronic myelogenous leukemia stem cells by histone deacetylase inhibitors in combination with imatinib mesylate. Cancer Cell 2010;18:427-42
  • Nemeth MJ, Mak KK, Yang Y, et al. beta-Catenin expression in the bone marrow microenvironment is required for long-term maintenance of primitive hematopoietic cells. Stem Cells 2009;27:1109-19
  • Zeng X, Tamai K, Doble B, et al. A dual-kinase mechanism for Wnt co-receptor phosphorylation and activation. Nature 2005;438:873-7
  • Hu Y, Chen Y, Douglas L, et al. beta-Catenin is essential for survival of leukemic stem cells insensitive to kinase inhibition in mice with BCR-ABL-induced chronic myeloid leukemia. Leukemia 2009;23:109-16
  • Heidel FH, Bullinger L, Feng Z, et al. Genetic and pharmacologic inhibition of β-Catenin targets imatinib-resistant leukemia stem cells in CML. Cell Stem Cell 2012;10:412-24
  • Seke Etet PF, Vecchio L, Nwabo Kamdje AH. Signaling pathways in chronic myeloid leukemia and leukemic stem cell maintenance: key role of stromal microenvironment. Cell Signal 2012;24:1883-8
  • Frassanito MA, Rao L, Moschetta M, et al. Bone marrow fibroblasts parallel multiple myeloma progression in patients and mice: in vitro and in vivo studies. Leukemia 2013, doi:10.1038/leu.2013.254
  • Lane SW, Scadden DT, Gilliland DG. The leukemic stem cell niche: current concepts and therapeutic opportunities. Blood 2009;114:1150-7
  • Damiano JS, Hazlehurst LA, Dalton WS. 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;15:1232-9
  • Solanilla A, El Andaloussi A, Grosset C, et al. Differential effect of interferon alpha on chronic myelogenous leukaemia and normal haematopoietic progenitors in a stromal cell co-culture context: role of the flt3 ligand. Br J Haematol 2000;109:382-7
  • Vianello F, Villanova F, Tisato V, 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;95:1081-9
  • Geay JF, Buet D, Zhang Y, et al. p210BCR-ABL inhibits SDF-1 chemotactic response via alteration of CXCR4 signaling and down-regulation of CXCR4 expression. Cancer Res 2005;65:2676-83
  • Jin L, Tabe Y, Konoplev S, et al. CXCR4 upregulation by imatinib induces chronic myelogenous leukemia (CML) cell migration to bone marrow stroma and promotes survival of quiescent CML cells. Mol Cancer Ther 2008;7:48-58
  • Devine SM, Vij R, Rettig M, et al. Rapid mobilization of functional donor hematopoietic cells without G-CSF using AMD3100, an antagonist of the CXCR4/SDF-1 interaction. Blood 2008;112:990-8
  • Weisberg E, Azab AK, Manley PW, et al. Inhibition of CXCR4 in CML cells disrupts their interaction with the bone marrow microenvironment and sensitizes them to nilotinib. Leukemia 2012;26:985-90
  • Agarwal A, Fleischman AG, Petersen CL, et al. Effects of plerixafor in combination with BCR-ABL kinase inhibition in a murine model of CML. Blood 2012;120:2658-68
  • Mohyeldin A, Garzón-Muvdi T, Quiñones-Hinojosa A. Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 2010;7:150-61
  • Eliasson P, Nsson J. The Hematopoietic stem cell niche: low in oxygen but a nice place to be. J Cell Physiol 2010;222:17-22
  • Zhang H, Li H, Xi HS, et al. HIF1alpha is required for survival maintenance of chronic myeloid leukemia stem cells. Blood 2012;119:2595-607
  • Helgason GV, Karvela M, Holyoake TL. Kill one bird with two stones: potential efficacy of BCR-ABL and autophagy inhibition in CML. Blood 2011;118:2035-43
  • Mathew R, Karantza-Wadsworth V, White E. Role of autophagy in cancer. Nat Rev Cancer 2007;7:961-7
  • Bellodi C, Lidonnici MR, Hamilton A, et al. Targeting autophagy potentiates tyrosine kinase inhibitor–induced cell death in Philadelphia chromosome–positive cells, including primary CML stem cells. J Clin Invest 2009;119:1109-23
  • Chen Y, Hu Y, Zhang H, et al. Loss of the Alox5 gene impairs leukemia stem cells and prevents chronic myeloid leukemia. Nat Genet 2009;41:783-92
  • Chen Y, Li D, Li S. The Alox5 gene is a novel therapeutic target in cancer stem cells of chronic myeloid leukemia. Cell Cycle 2009;8:3488-92
  • Hogdal LJ, Letai A. BCL-2 inhibition – stemming the tide of myeloid malignancies. Cell Stem Cell 2013;12:269-70
  • Juin P, Geneste O, Gautier F, et al. Decoding and unlocking the BCL2 dependency of cancer cells. Nat Rev Cancer 2013;13:455-65
  • Goff DJ, Recart AC, Sadarangani A, et al. A Pan-BCL2 inhibitor renders bone-marrow-resident human leukemia stem cells sensitive to tyrosine kinase inhibition. Cell Stem Cell 2013;12:316-28
  • Neviani P, Harb JG, Oaks JJ, et al. PP2A-activating drugs selectively eradicate TKI-resistant chronic myeloid leukemic stem cells. J Clin Invest 2013;123:4144-57
  • Reddiconto G, Toto C, Palamà I, et al. Targeting of GSK3b promotes imatinib-mediated apoptosis in quiescent CD34+ chronic myeloid leukemia progenitors, preserving normal stem cells. Blood 2012;119:2335-234
  • Nelson EA, Walker SR, Weisberg E, et al. The STAT5 inhibitor pimozide decreases survival of chronic myelogenous leukemia cells resistant to kinase inhibitors. Blood 2011;117:3421-9
  • Walz C, Ahmed W, Lazarides K, et al. Essential role for Stat5a/b in myeloproliferative neoplasms induced by BCR-ABL1 and JAK2V617F in mice. Blood 2012;119:3550-60
  • Chen M, Gallipoli P, DeGeer D, et al. Targeting primitive chronic myeloid leukemia cells by effective inhibition of a new AHI-1–Bcr-ABl–JAK2 complex. J Natl Cancer Inst 2013;105:405-23
  • Pellicano F, Šimara P, Sinclair A, et al. The MEK inhibitor PD184352 enhances BMS-214662-induced apoptosis in CD34+ CML stem/progenitor cells. Leukemia 2011;25:1159-67
  • Lord CJ, Ashworth A. The DNA damage response and cancer therapy. Nature 2012;481:287-94
  • Curtin NJ. DNA repair dysregulation from cancer driver to therapeutic target. Nat Rev Cancer 2012;12:801-17
  • Chakraborty S, Stark JM, Sun CL, et al. Chronic myelogenous leukemia stem and progenitor cells demonstrate chromosomal instability related to repeated breakage-fusion-bridge cycles mediated by increased nonhomologous end joining. Blood 2012;119:6187-97
  • Bolton-Gillespie E, Schemionek M, Klein HU, et al. Genomic instability may originate from imatinib-refractory chronic myeloid leukemia stem cells. Blood 2013;121:4175-83
  • Cramer-Moralesv K, Nieborowska-Skorska M, Scheibner K, et al. Personalized synthetic lethality induced by targeting RAD52 in leukemias identified by gene mutation and expression profile. Blood 2013;122:1293-304
  • Wetzler M, Donohue KA, Odenike OM, et al. Feasibility of administering oblimersen (G3139; Genasense) with imatinib mesylate in patients with imatinib resistant chronic myeloid leukemia–cancer and leukemia group B study 10107. Leuk Lymphoma 2008;49:1274-8

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