Targeting the acute myeloid leukemia stem cells

Anti-Cancer Agents in Medicinal Chemistry

Volumn 10, Issue 2, 2010, Pages 104-110

  Krause, Alexandre ^a   Fontanari Krause, Luciana M ^a   Rego, Eduardo M ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Acute myeloid leukemia; Bone marrow microenvironment; Leukemia stem cells

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; AZACITIDINE; BCR ABL PROTEIN; BETA CATENIN; BIOLOGICAL MARKER; BMI1 PROTEIN; BORTEZOMIB; CHEMOKINE RECEPTOR CXCR4 ANTAGONIST; CYCLIN DEPENDENT KINASE INHIBITOR 2A; DASATINIB; EVEROLIMUS; FLT3 LIGAND; GRANULOCYTE COLONY STIMULATING FACTOR; GRN 163L; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 2; LESTAURTINIB; MIDOSTAURIN; MULTIDRUG RESISTANCE PROTEIN 1; N [1,4,8,11 TETRAAZACYCLOTETRADECANYL 1,4 PHENYLENEBIS(METHYLENE)] 2 (AMINOMETHYL)PYRIDINE; NERVE CELL ADHESION MOLECULE; PARTHENOLIDE; RAPAMYCIN; SALINOSPORAMIDE A; STROMAL CELL DERIVED FACTOR 1; TDZD 8; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; TEMSIROLIMUS; UNCLASSIFIED DRUG; UNINDEXED DRUG; VORINOSTAT; ZOSUQUIDAR;

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LYMPHOCYTIC LEUKEMIA; APOPTOSIS; B LYMPHOCYTE; BLAST CELL CRISIS; BONE MARROW; CANCER REGRESSION; CANCER STEM CELL; CANCER THERAPY; CELL CYCLE; CELL DIVISION; CELL FATE; CELL INFILTRATION; CELL RENEWAL; CELL SUBPOPULATION; CELL SURVIVAL; CELL TRANSFORMATION; CHRONIC LYMPHATIC LEUKEMIA; CHRONIC MYELOID LEUKEMIA; DRUG MECHANISM; HEMATOPOIETIC STEM CELL; IMMUNOPHENOTYPING; LEUKEMIA CELL; MICROENVIRONMENT; MONOCYTE; MULTIDRUG RESISTANCE; MULTIPLE MYELOMA; NONHODGKIN LYMPHOMA; NONHUMAN; PROMYELOCYTIC LEUKEMIA; PROTEIN EXPRESSION; PROTEIN STABILITY; PROTEIN TARGETING; REVIEW; SCID MOUSE; TARGET CELL; TELOMERE; TRANSCRIPTION INITIATION;

EID: 77950796977     PISSN: 18715206     EISSN: None     Source Type: Journal    
DOI: 10.2174/187152010790909281     Document Type: Review

References (92)

1. Griffin, J.D.; Löwenberg, B. Clonogenic cells in acute myeloblastic leukemia. Blood, 1986, 68(6), 1185-1195.
2. McCulloch, E.A.; Till, J.E. Blast cells in acute myeloblastic leukemia: a model. Blood Cells, 1981, 7(1), 63-77.
3. Lapidot, T.; Sirard, C.; Vormoor, J.; Murdoch, B.; Hoang, T.; Caceres-Cortes, J.; Minden, M.; Paterson, B.; Caligiuri, M.A.; Dick, J.E. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature, 1994, 367, 645-648.
4. Bonnet, D. Leukemic stem cells show the way. Folia Histochem. Cytobiol., 2005, 43(4), 183-186. (Pubitemid 41582135)
5. Bonnet, D.; Dick, J.E. Human acute leukemia is organized as a hierarchy that originates from a primitive hematopoietic stem cell. Nat. Med., 1997, 3(7), 730-737.
6. Hope, K.; Jin, L.; Dick, J.E. Acute myeloid leukemia originates form a hierarchy of leukemic stem cell classes that differ in selfrenewal capacity. Nat. Immunol., 2004, 5, 738-743.
7. Terspstra, W.; Ploemacher, R.E.; Prins, A.; Van Lom, K.; Pouwels, K.; Wognum, A.W., Wagemaker, G.; Lowenberg, B.; Wielenga, J.J. Fluorouracil selectively spares acute myeloid leukemia cells with long-term growth abilities in immunodeficient mice in culture. Blood, 1996, 88, 1944-1950. (Pubitemid 26307894)
8. Guzman, M.L.; Neering, S.J.; Upchurch, D.; Grimes, B.; Howard, D.S.; Rizzieri, D.A.; Luger, S.M.; Jordan, C.T. Nuclear factor-κβ is constitutively activated in primitive human acute myelogenous leukemia cells. Blood, 2001, 98(8), 2301-2307.
9. Xu, Q.; Simpson, S.E.; Scialla, T.J.; Bagg, A.; Carroll, M. Survival of acute myeloid leukemia cells requires PI3 kinase activation. Blood, 2003, 102(3), 972-980.
10. Xu, Q.; Thompson, J.E., Carroll, M. mTOR regulates cell survival after etoposide treatment in primary AML cells. Blood, 2005, 106(13), 4261-4268.
11. Jordan, C.T.; Upchurch, D.; Szilvassy, S.J.; Guzman, M.L.; Howard, D.S.; Pettigrew, A.L.; Meyerrose, T.; Rossi, R.; Grimes, B.; Rizzieri, D.A.; Luger, S.M.; Phillips, G.L. The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells. Leukemia, 2000, 14(10), 1777-1784.
12. Taussig, D.C.; Pearce, D.J.; Simpson, C.; Rohatiner, A.Z.; Lister, T.A.; Kelly, G.; Luongo, J.L.; Danet-Desnoyers, G.A.; Bonnet, D. Hematopoietic stem cells express multiple myeloid markers: implications for the origin and targeted therapy of acute myeloid leukemia. Blood, 2005, 106(13), 4086-4092.
13. Van Rhenen, A.; van Dongen, G.A.; Kelder, A.; Rombouts, E.J.; Feller, N.; Moshaver, B.; Stigter-van Walsum, M.; Zweegman, S.; Ossenkoppele, G.J.; Jan Schuurhuis, G. The novel AML stem cell associated antigen CLL-1 aids in discrimination between normal and leukemic stem cells. Blood, 2007, 110(7), 2659-2666.
14. Guibal, F.C.; Alberich-Jorda, M.; Hirai, H.; Ebralidze, A.; Levantini, E.; Di Ruscio, A.; Zhang, P.; Santana-Lemos, B.A.; Neuberg, D.; Wagers, A.J.; Rego, E.M.; Tenen, D.G. Identification of a myeloid committed progenitor as the cancer initiating cell in acute promyelocytic leukemia. Blood, 2009, 114(27), 5415-5425.
15. Krivtsov, A.V.; Twomey, D.; Feng, Z.; Stubbs, M.C.; Wang, Y.; Faber, J.; Levine, J.E.; Wang, J.; Gilliland, D.G.; Golub, T.R.; Armstrong, S.A. Transformation from committed progenitor to leukemia stem cell initiated by MLL-AF9. Nature, 2006, 442, 818-822.
16. Somervaille, T.C.; Cleary, M.L. Identification and characterization of leukemia stem cells in murine MLL-AF9 acute myeloid leukemia. Cancer Cell, 2006, 10(4), 257-268.
17. Wei, J.; Wunderlich, M.; Fox, C.; Alvarez, S.; Cigudosa, J.C.; Wilhelm, J.S.; Zheng, Y.; Cancelas, J.A.; Gu, Y; Jansen, M.; Dimartino, J.F.; Mulloy, J.C. Microenvironment determines lineage fate in a human model of MLL-AF9 leukemia. Cancer Cell, 2008, 13, 483-485.
18. Deshpande, A.J.; Cusan, M.; Rawat, V.P.; Reuter, H.; Krause, A.; Pott, C.; Quintanilla-Martinez, L.; Kakadia, P.; Kuchenbauer, F.; Ahmed, F.; Delabese, E.; Lichter, P.; Kneba, M.; Hiddemann, W.; Macintyer, E.; Mecucci, C.; Ludwig, W.D.; Humphries, R.K.; Bohlander, S.K.; Feuring-Buske, M.; Buske, C. Acute myeloid leukemia is propagated by a leukemic stem cell with lymphoid characteristics in a mouse model of CALM/AF10-positive leukemia. Cancer Cell, 2006, 10, 363-374.
19. Lessard, J.; Sauvageau, G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature, 2003, 423, 255-260.
20. Yilmaz, O.H.; Valdez, R.; Theisen, B.K.; Guo, W.; Ferguson, D.O.; Wu, H.; Morrison, S.J. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature, 2006, 441(7092), 475-482. (Pubitemid 44050144)
21. Wang, J.C.; Dick, J.E. Cancer stem cells: lessons from leukemia. Trends Cell Biol., 2005, 15, 494-501.
22. Eisterer, W.; Jiang, X.; Christ, O.; Glimm, H.; Lee, K.H.; Pang, E.; Lambie, K.; Shaw, G.; Holyoake, T.L.; Petzer, A.L.; Auewarakul, C.; Barnett, M.J.; Eaves, C.J.; Eaves, A.C. Different subsets of primary chronic myeloid leukemia stem cells engraft immunodeficient mice and produce a model of the human disease. Leukemia, 2005, 19(3), 435-441.
23. Hu, Y.; Swerdlow, S.; Duffy, T.M.; Weinmann, R.; Lee, F.Y.; Li, S. Targeting multiple kinase pathways in leukemic progenitors and stem cells is essential for improved treatment of Ph+ leukemia in mice. Proc Natl. Acad. Sci. USA, 2006, 103(45), 16870-16875.
24. Neering, S.J.; Bushnell, T.; Sozer, S.; Ashton, J.; Rossi, R.M.; Wang, P.Y.; Bell, D.R.; Heinrich, D.; Bottaro, A.; Jordan, C.T. Leukemia stem cells in a genetically defined murine model of blast-crisis CML. Blood, 2007, 110(7), 2578-2585.
25. Krause, D.S.; Lazarides, K.; von Andrian, U.H.; Van Etten, R.A. Requirement for CD44 in homing and engraftment of BCR-ABLexpressing leukemic stem cells. Nat. Med., 2006, 12(10), 1175-1180.
26. Jamieson, C.H.M.; Ailles, L.E.; Dylla, S.J.; Muijtjens, M.; Jones, C.; Zehnder, J.L.; Gotlib, J.; Li, K.; Manz, M.G.; Keating, A.; Sawyers, C.L.; Weissman, I.L. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N. Engl. J. Med., 2004, 351(7), 634-636.
27. Dash, A.B.; Williams, I.R.; Kutok, J.L.; Tomasson, M.H.; Anastasiadou, E.; Lindahl, K.; Li, S.; Van Etten, R.A.; Borrow, J.; Housman, D.; Druker, B.; Gilliland, D.G. A murine model of CML blast crisis induced by cooperation between BCR/ABL and NUP98/HOXA9. Proc Natl. Acad. Sci. USA, 2002, 99(11), 7622-7627.
28. Miyamoto, T.; Weissman, I.L.; Akashi, K. AML1/ETO-expressing nonleukemic stem cells in acute myelogenous leukemia with 8,21 chromosomal translocation. Proc Natl. Acad. Sci. USA, 2000, 20(13), 7521-7526.
29. Cozzio, A.; Passegué, E.; Ayton, P.M.; Karsunky, H.; Cleary, M.L.; Weissmann, I.L. Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev., 2003, 17, 3029-3035.
30. Huntly, B.J.; Shigematsu, H.; Deguchi, K.; Lee, B.H.; Mizuno, S.; Duclos, N.; Rowan, R.; Amaral, S.; Curley, D.; Williams, I.R.; Akashi, K.; Gilliland, D.G. MOZ-TIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell, 2004, 6, 587-596.
31. Passegué, E.; Jamieson, C.H.M.; Ailles, L.E.; Weissman, I.L. Normal and leukemic hematopoiesis: Are leukemias a stem cell disorder or a reacquisition if stem cell characteristics? Proc Natl. Acad. Sci. USA, 2003, 100(1), 11842-11849.
32. Turhan, A.G.; Lemoine, F.M.; Debert, C.; Bonnet, M.L.; Baillo, C.; Picard, F.; Macintyre, E.A.; Varet, B. Highly purified primitive hematopoietic stem cells are PML-RARA negative and generate monoclonal progenitors in acute promyelocytic leukemia. Blood, 1995, 85, 2154-2161.
33. Westervelt, P.; Ley, T.J. Seed versus soil: The importance of the target cell for transgenic models of human leukemias. Blood, 1999, 93, 2143-2148.
34. Rego, E.M.; Ruggero, D.; Tribioli, C.; Cattoretti, G.; Kogan, S.; Redner, R.L.; Pandolfi, P.P. Leukemia with distinct phenotypes in transgenic mice expressing PML/RAR alpha, PLZF/RAR alpha or NPM/RAR alpha. Oncogene, 2006, 25(13), 1974-1979.
35. Gil, J.; Bernard, D.; Peters, G. Role of polycomb group proteins in stem cell self-renewal and cancer. DNA Cell Biol., 2005, 24(2), 117-125.
36. Andreeff, M.; Ruvolo, V.; Gadgil, S.; Zeng, C.; Coombes, K.; Chen, W.; Kornblau, S.; Barón, A.E.; Drabkin, H.A. HOX expression patterns identify a common signature for favorable AML. Leukemia, 2008, 22(11), 2041-2047.
37. Rizzo, A.A.; Olthof, S.; Han, L.; Vellenga, E.; de Haan, G.; Schuringa, J.J. Repression of BMI1 in normal and leukemic human CD34+ cells impairs self-renewal and induces apoptosis. Blood, 2009, 114(8), 1498-1505.
38. Warner, J.K.; Wang, J.C.Y.; Takenaka, K.; Doulatov, S.; McKenzie, J.L.; Harrington, L.; Dick, J.E. Direct evidence for co operating genetic events in the leukemic transformation of normal human hematopoietic cells. Leukemia, 2005, 19, 1794-1805.
39. Calado, R.T.; Regal, J.A.; Hills, M.; Yewdell, W.T.; Dalmazzo, L.F.; Zago, M.A.; Landsdorp, P.M.; Hogge, D.; Chanock, S.J.; Estey, E.H.; Falcão, P.R.P.; Young, N. Constitutional hypomorphic telomerase mutations in patients with acute myeloid leukemia. Proc Natl. Acad. Sci. USA, 2008, 106(4), 1187-1192.
40. Weisberg, E.; Barrett, R.; Liu, Q.; Stone, R.; Gray, N.; Griffin, J.D. FLT3 inhibition and mechanisms of drug resistance in mutant FLT3-positive AML. Drug Resist. Updat., 2009, 12, 81-89.
41. Schlenk, R.F.; Döhner, K. Impact of new prognostic markers in treatment decisions in acute myeloid leukemia. Curr. Opin. Hematol., 2009, 16, 98-104.
42. Levis, M.; Murphy, K.M.; Pham, R.; Kim, K.T.; Stine, A.; Li, L.; McNiece, I.; Smith, B.D.; Small, D. Internal tandem duplications of the FLT3 gene are present in leukemia stem cells. Blood, 2005, 106(2):673-680
43. Griessinger, E.; Frelin, C.; Cuburu, N.; Imbert, V.; Dageville, C.; Hummelsberger, M.; Sirvent, N.; Dreano, M.; Peyron, J.F. Preclinical targeting of NF-κβ and FLT3 pathways in AML cells. Leukemia, 2008, 22, 1466-1469.
44. Ito, K.; Bernardi, R.; Pandolfi, P.P. 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, 51-59.
45. Bjornsti, M.A.; Houghton, P.J. The TOR pathway: A target for cancer therapy. Nat. Rev., 2004, 4, 335-348.
46. Figueiredo-Pontes, L.L.; Pintão, M.-C.T.; Oliveira, L.C.O.; Dalmazzo, L.F.F.; Jácomo R.H.; Garcia A.B.; Falcão R.P.; Rego E.M. Determination of P-Glycoprotein, MDR-related protein 1, breast cancer resistance protein, and lung-resistance protein expression in leukemic stem cells of acute myeloid leukemia. Cytometry Part B, 2008, 74B, 163-168..
47. Ayala, F.; Dewar, R.; Kieran, M.; Kalluri, R. Contribution of bone microenvironment to leukemogenesis and leukemia progression. Leukemia, 2009, 23(12), 2233-2241.
48. Nilsson, S.K.; Hayley, M.J.; Coverdale, J.A.; Spatial localization of transplanted hematopoietic stem cells: inferences for the localization of stem cell niches. Blood, 2001, 97, 2293-2299.
49. Perry, J.M.; Li, L. Disrupting the stem cell niche: good seeds in bad soil. Cell, 2007, 129, 1045-1047.
50. Calvi, L.M.; Adams, G.B.; Weibrecht, K.W.; Weber, J.M.; Olson, D.P.; Knight, M.C.; Martin, R.P.; Dicieti, S.E.; Bringhurst, F.R.; Miner, L.A.; Kronenberg, H.M.; Scaden, D.T. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature, 2003, 425(6960), 841-846.
51. Raaijimakers, M.H.P.; Scadden, D.T. Evolving concepts on the microenvironmental niche for hematopoietic stem cells. Curr. Opin. Hematol., 2008, 15, 301-306.
52. Weber, J.M.; Calvi, L.M. Notch signaling and the bone marrow hematopoietic stem cell niche. Bone, 2010, 46(2), 281-285.
53. Schwanbeck, R.; Schroeder T.; Henning, K.; Kohlhof, H.; Rieber, N.; Erfurth M.L.; Just, U. Notch Signaling in Embryonic and Adult Myelopoiesis. Cells Tissues Organs, 2008, 188, 91-102.
54. Lane, S.W.; Scadden, D.T.; Gilliland, D.G. The leukemic stem cell niche: current concepts and therapeutic opportunities. Blood, 2009, 114, 1150-1157.
55. Nemeth, M.J.; Bodine; D.M. Regulation of hematopoiesis and the hematopoietic stem cell niche by Wnt signaling pathways. Cell Res., 2007, 17, 746-758.
56. Zhang, J.; Niu, C.; Ye, L.; Huang, H.; He, X.; Tong, W.G.; Ross, J.; Haug, J.; Jonhson, T.; Feng, J.Q.; Harris, S.; Wiedemann, L.M.; Mishina, Y.; Li, L. Identification of the haematopoietic stem cell niche and control of the niche size. Nature, 2003, 425(6960), 836-841.
57. Kiel, M.J.; Acar, M.; Radice, G.L.; Morrison, S.J. Hematopoietic stem cells do not depend on N-cadherin to regulate their maintenance. Cell Stem Cell, 2009, 4(2), 170-179.
58. Avigdor, A.; Goichberg, P.; Shivtiel, S.; Dar, A.; Peled, A.; Samira, S.; Kollet, O.; Hershkoviz, R.; Alon, R.; Hardan, I.; Ben-Hur, H.; Naor, D.; Nagler, A.; Lapidot, T. CD44 and hyaluronic acid cooperate with SDF-1 in the trafficking of human CD34+ stem/progenitor cells to bone marrow. Blood, 2004, 103(8), 2981-2989.
59. Tavernier-Tardy, E.; Cornillon, J.; Campos, L.; Flandrin, P.; Duval, A.; Nadal, N.; Guyotat, D. Prognostic value of CXCR4 and FAK expression in acute myelogeneous leukemia. Leuk. Res., 2009, 33, 764-768.
60. Rombouts, E.J.C.; Pavic, B.; Löwenberg, B.; Ploemacher, R.E. Relation between CXCR-4 expression, Flt3 mutations, and unfavorable prognosis of adult acute myeloid leukemia. Blood, 2004, 104(2), 550-557.
61. Tavor, S.; Petit, I.; Porozov, S.; Avigdor, A.; Dar A.; Leider-Trejo, L.; Shemtov, N.; Deutsch, V.; Naparstek, E.; Nagler, A.; Lapidot, T. CXCR4 regulates migration and development of human acute myelogenous leukemia stem cells in transplanted NOD/SCID mice. Cancer Res., 2004, 64(8), 2817-2824.
62. Tavor, S.; Eisenbach, M.; Jacob-Hirsch, J.; Golan, T.; Petit, I.; BenZion, K.; Kay, S.; Baron, S.; Amariglio, N.; Deutsch, V.; Naparstek, E.; Rechavi, G. The CXCR4 antagonist AMD3100 impairs survival of human AML cells and induces their differentiation. Leukemia, 2008, 22, 2151-2158.
63. Zeng, Z.; Shi, Y.X.; Samudio, I.J.; Wang, R.Y.; Ling, X.; Frolova, O.; Levis, M.; Rubin, J.B.; Negrin, R.R.; Estey, E.H.; Konoplev, S.; Andreeff, M.; Konopleva, M. Targeting the leukemia microenvironment by CXCR4 inhibition overcomes resistance to kinase inhibitors and chemotherapy in AML. Blood, 2009, 113(24), 6215-6224.
64. Ramirez, P.; Rettig, M.P.; Uly, G.L.; Deych, E.; Holt, M.S.; Ritchey, J.K.; DiPersio, J.F. BIO5192, a small molecule inhibitor of VLA-4, mobilizes hematopoietic stem and progenitor cells. Blood, 2009, 114(7), 1340-1343.
65. Williams, C.K.; Segarra, M.; Sierra, M.D.L.; Sainson, R.C.A.; Tosato, G.; Harris, A.L. Regulation of CXCR4 by the notch ligand delta-like 4 in endothelial. Cells. Cancer Res., 2008, 68(6), 1889-1895.
66. Rao, S.S.; O'Neil, J.; Liberator, C.D.; Hardwick, J.S.; Dai, X.; Zhang, T.; Tyminsdi, E.; Yuan, J.; Kohl, N.E.; Richon, V.M.; Van der Ploeg, L.H.; Carroll, P.M.; Draetta, G.F.; Look, A.T.; Strack, P.R.; Winter, C.G. Inhibition of NOTCH signaling by gamma secretase inhibitor engages the RB pathway and elicits cell cycle exit in T-cell acute lymphoblastic leukemia cells. Cancer Res., 2009, 69(7), 3060-3068.
67. Lancet, J.E.; Baer, M.R.; Duran, G.E.; List, A.F.; Fielding, R.; Marcelletti, J.F.; Multani, P.S.; Sikic, B.I. A phase I trial of continuous infusion of the multidrug resistance inhibitor zosuquidar with daunorubicin and cytarabine in acute myeloid leukemia. Leuk. Res., 2009, 33(8), 1055-1061.
68. Zhang, Y.; Rowley, J.D. Chromatin structural elements and chromosomal translocations in leukemia. DNA Repair, 2006, 5, 1282-1297.
69. Ito, K.; Bernardi, R.; Morotti, A.; Matsuoka, S.; Saglio, G.; Ikeda, Y.; Rosenblatt, J.; Avigan, D.E.; Teruya-Feldstein, J.; Pandolfi, P.P. PML targeting eradicates quiescent leukaemia-initiating cells. Nature, 2008, 453, 1072-1078.
70. Krause, D.S.; Van Etten, R.A. Interfering with leukemic stem cells. Nat. Med., 2008, 14(1), 494-495.
71. Visani, G.; Piccaluga, P.; Malagola, M.; Isidori, A. Efficacy of dasatinib in conjunction with α-interferon for the treatment of imatinib-resistant and dasatinib-resistant Ph+ acute lymphoblastic leukemia. Leukemia, 2009, 23, 1687-1688.
72. Passegué, E.; Ernst, P. IFN-α wakes up sleeping hematopoietic stem cells. Nat. Med., 2009, 15(6), 612-613.
73. Sato, T.; Onai, N.; Yoshihara, H.; Arai, F.; Suda, T.; Ohteki, T. Interferon regulatory factor-2 protects quiescent hematopoietic stem cells from type I interferon-dependent exhaustion. Nat. Med., 2009, 15(6), 696-700.
74. Essers, M.A.G.; Offner, S.; Blanco-Bose, W.E.; Waibler, Z.; Kalinke, U.; Duchosal, M.A.; Trump, A. IFNα activates dormant haematopoietic stem cells in vivo. Nature, 2009, 458, 904-908.
75. Nasr, R.; Guillemin, M.C.; Ferhi, O.; Soilihi, H.; Peres, L.; Berthier, C.; Rousselot, P.; Robledo-Sarmiento, M.; Lallemand-Breitenbach, V.; Gourmel, B.; Vitoux, D.; Pandolfi, P.P.; Rochette-Egly, C.; Zhu, J.; deThé, H. Eradication of acute promyelocytic leukemia-initiating cells through PML-RAR degradation. Nat. Med., 2008, 14(12), 1333-1342.
76. Nasr, R.; Lallemand-Breitenbach, V.; Zhu, J.; Guillemin, M.C.; de Thé, H. Therapy-induced PML-RARA proteolysis and acute promyelocytic leukemia cure. Clin. Cancer Res., 2009, 15, 6321-6326.
77. Brummendorf, T.H.; Balabanov, S. Telomere length dynamics in normal hematopoiesis and in disease states characterized by increased stem cell turnover. Leukemia, 2006, 20, 1706-1716.
78. Hiyama, E.; Hiyama, K. Telomere and telomerase in stem cells. Br. J. Cancer, 2007, 96, 1020-1024.
79. Shammas, M.A.; Koley, H.; Bertheau, R.C.; Neri, P.; Fulciniti, M.; Tassone, P.; Blotta, S.; Protopopov, A.; Mitsiades, C.; Batchu, R.B.; Anderson, K.C.; Chin, A.; Gryaznov, S.; Munshi, N.C. Telomerase inhibitor GRN163L inhibits myeloma cell growth in vitro and in vivo. Leukemia, 2008, 22(7), 1410-1418.
80. Danet-Desnoyers, G.A.; Luongo, I.L.; Bonnet, D.A.; Domchek, S.M., Vonderheide, R.H. Telomerase vaccination has no detectable effect on SCID-repopulating and colony-forming activities in the bone marrow of cancer patients. Exp. Hematol., 2005, 33, 1275-1280.
81. Yee, K.W.; Zeng, Z.; Konopleva, M.; Verstovsek, S.; Ravandi, F.; Ferrajoli, A.; Thomas, D.; Wierda, W.; Apostolidou, E.; Albitar, M.; O'Brien, S.; Andreeff, M.; Giles, F.J. Phase I/II study of the mammalian target of rapamycin inhibitor everolimus(RAD001) in patients with relapsed or refractory hematologic malignancies. Clin. Cancer Res., 2006, 12, 5165-5173.
82. Perl, A.E.; Kasner, M.T.; Tsai, D.E.; Vogl, D.T.; Loren, A.W.; Schuster, S.J.; Porter, D.L.; Stadtmauer, E.A.; Goldstein, S.C.; Frey, N.V.; Nasta, S.D.; Hexner, E.O.; Dierov, J.K.; Swider, C.R.; Bagg, A.; Gewirtz, A.M.; Carroll, M.; Luger, S.M. A Phase I study of the mammalian target of rapamycin inhibitor sirolimus and MEC chemotherapy in relapsed and refractory acute myelogenous leukemia. Clin. Cancer Res., 2009, 15(21), 6732-6739.
83. Schaefer, E.W.; Loaiza-Bonilla, A.; Juckett, M.; DiPersop, J.F.; Roy, V.; Slack, J.; Wu, W.; Laumann, K.; Espinoza-Delgado, I.; Gore, S.D. A phase 2 study of vorinostat in acute myeloid leukemia. Haematologica, 2009, 94(10), 1375-1382.
84. Ravandi, R.; Issa, J.P.; Garcia-Manero, G.; O'Brien, S.; Pierce, S.; Shan, J..; Borthakur, G.; Verstovsek, S.; Faderl, S.; Cortes, J.; Kantarjian, H. Superior outcome with hypomethylating therapy with acute myeloid leukemia and high-risk myelodysplastic syndrome and chromosome 5 and 7 abnormalities. Cancer, 2009, 115, 5746-5751.
85. Knapper, S.; Burnett, A.K.; Littlewood, T.; Kell, W.J.; Agrawal, S.; Chopra, R.; Clark, R.; Lewis, MJ.; Small, D. A phase 2 trial of the FLT3 inhibitor lestaurtinib(CEP701) as first-line treatment for older patients with acute myeloid leukemia not considered fit for intensive chemotherapy. Blood, 2006, 108, 3262-3270.
86. Sanz, M.; Burnett, A.; Lo-Coco, F.; Löwenberg, B. FLT3 inhibition as a targeted therapy for acute myeloid leukemia. Curr. Opin. Oncol., 2009, 21(6), 594-600.
87. Stone, R.M.; DeAngelo, D.J.; Klimek, V.; Gallinsky, I.; Estey, E.; Nimer, S.D.; Grandin, W.; Lebwohl, D.; Wang, Y.; Cohen, P.; Fox, E.A.; Neuberg, D.; Clark, J.; Gilliland, D.G.; Griffin, J.D. Patients with acute myeloid leukemia and an activating mutation in FLT3 tyrosine kinase inhibitor, PKC412. Blood, 2005, 105(V), 54-60.
88. Crazzolara, R.; Bradstock, K.F.; Bendall, L.J. RAD001(Everolimus) induces autophagy in acute lymphoblastic leukemia. Authophagy, 2009, 5(5), 727-728.
89. Fracasso, P.M.; Goldstein, L.J.; de Alwis, D.P.; Rader, J.S.; Arquette, M.A.; Goodner, S.A.; Wright, L.P.; Fears, C.L.; Gazak, R.J.; Andre, V.A.; Slapak, C.A.; Schellens, J.H. Phase I study of docetaxel in combination with the P-glycoprotein inhibitor, zosuquidar in resistant malignancies. Clin. Cancer Res., 2004, 10, 7220-7228.
90. Miller, C.P.; Ban, K.; Dujka, M.E.; McConkey, D.J.; Munsell, M.; Palladino, M.; Chandra, J. NPI-0052, a novel proteasome inhibitor, induces caspase-8 and ROS-dependent apoptosis alone and in combination with HDAC inhibitors in leukemia cells. Blood, 2007, 110(1), 267-277.
91. Ruiz, S.; Krupnik, 'Y.; Keating, M. The proteasome inhibitor NPI-0052 is a more effective inducer of apoptosis than bortezomib in lymphocytes from patients with chronic lymphocytic leukemia. Mol. Cancer Ther., 2006, 5, 1836-1843.
92. Jordan, C.T. The leukemic stem cell. Best Pract. Res. Clin. Haematol., 2007, 20, 13-18.