Kill one bird with two stones: Potential efficacy of BCR-ABL and autophagy inhibition in CML

Blood

Volumn 118, Issue 8, 2011, Pages 2035-2043

  Helgason, G Vignir ^a   Karvela, Maria ^a   Holyoake, Tessa L ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLADENINE; AMMONIUM CHLORIDE; ARSENIC TRIOXIDE; BAFETINIB; BAFILOMYCIN A1; BCR ABL PROTEIN; BORTEZOMIB; BOSUTINIB; CHLOROQUINE; DASATINIB; DCC 2036; GRANULOCYTE COLONY STIMULATING FACTOR; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; GUANINE NUCLEOTIDE EXCHANGE FACTOR; HYDROXYCHLOROQUINE; IMATINIB; JANUS KINASE; MITOGEN ACTIVATED PROTEIN KINASE; NILOTINIB; PANOBINOSTAT; PHOSPHATIDYLINOSITOL 3 KINASE; PONATINIB; PROTEIN KINASE B; PROTEIN KINASE INHIBITOR; PROTEIN TYROSINE KINASE INHIBITOR; RAS PROTEIN; STAT5 PROTEIN; UNCLASSIFIED DRUG; UNINDEXED DRUG; VALPROIC ACID; WORTMANNIN; ZILEUTON;

AGING; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; AUTOPHAGY; CANCER CHEMOTHERAPY; CANCER SURVIVAL; CARCINOGENESIS; CELL DEATH; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CELL PROTECTION; CELL SURVIVAL; CHRONIC MYELOID LEUKEMIA; DISEASE COURSE; DISEASE SEVERITY; DRUG WITHDRAWAL; FEEDBACK SYSTEM; GENE MUTATION; HOMEOSTASIS; HUMAN; IMMUNITY; INFECTION; NEOPLASM; NERVE DEGENERATION; NONHUMAN; OVERALL SURVIVAL; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; QUALITY CONTROL; RECURRENCE RISK; REMISSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; STEM CELL; STEM CELL TRANSPLANTATION;

EID: 80052164677     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-01-330621     Document Type: Review

References (91)

1. Nowell PC, Hungerford DA. Chromosome studies on normal and leukemic human leukocytes. J Natl Cancer Inst. 1960;25:85-109.
2. Rowley JD. Letter: A new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature. 1973;243(5405):290-293.
3. Groffen J, Stephenson JR, Heisterkamp N, de Klein A, Bartram CR, Grosveld G. Philadelphia chromosomal breakpoints are clustered within a limited region, bcr, on chromosome 22. Cell. 1984;36(1):93-99.
4. Konopka JB, Watanabe SM, Witte ON. An alteration of the human c-abl protein in K562 leukemia cells unmasks associated tyrosine kinase activity. Cell. 1984;37(3):1035-1042.
5. Daley GQ, Van Etten RA, Baltimore D. Induction of chronic myelogenous leukemia in mice by the P210bcr/abl gene of the Philadelphia chromosome. Science. 1990;247(4944):824-830.
6. Daley GQ, Baltimore D. Transformation of an interleukin 3-dependent hematopoietic cell line by the chronic myelogenous leukemia-specific P210bcr/abl protein. Proc Natl Acad Sci U S A. 1988;85(23):9312-9316.
7. Deininger MW, Goldman JM, Melo JV. The molecular biology of chronic myeloid leukemia. Blood. 2000;96(10):3343-3356.
8. Pane F, Frigeri F, Sindona M, et al. Neutrophilicchronic myeloid leukemia: a distinct disease with a specific molecular marker (BCR/ABL with C3/A2 junction). Blood. 1996;88(7):2410-2414.
9. Li S, Ilaria RL Jr, Million RP, Daley GQ, Van Etten RA. 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. 1999;189(9):1399-1412.
10. Pendergast AM, Quilliam LA, Cripe LD, et al. BCR-ABL-induced oncogenesis is mediated by direct interaction with the SH2 domain of the GRB-2 adaptor protein. Cell. 1993;75(1):175-185.
11. Puil L, Liu J, Gish G, et al. Bcr-Abl oncoproteins bind directly to activators of the Ras signalling pathway. EMBO J. 1994;13(4):764-773.
12. Vivanco I, Sawyers CL. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer. 2002;2(7):489-501.
13. Skorski T, Kanakaraj P, Nieborowska-Skorska M, et al. Phosphatidylinositol-3 kinase activity is regulated by BCR/ABL and is required for the growth of Philadelphia chromosome-positive cells. Blood. 1995;86(2):726-736.
14. Salomoni P, Condorelli F, Sweeney SM, Calabretta B. Versatility of BCR/ABL-expressing leukemic cells in circumventing proapoptotic BAD effects. Blood. 2000;96(2):676-684.
15. Trotta R, Vignudelli T, Candini O, et al. BCR/ABL activates mdm2 mRNA translation via the La antigen. Cancer Cell. 2003;3(2):145-160.
16. Nave BT, Ouwens M, Withers DJ, Alessi DR, Shepherd PR. Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochem J. 1999;344 Pt 2:427-431.
17. Mohi MG, Boulton C, Gu TL, et al. Combination of rapamycin and protein tyrosine kinase (PTK) inhibitors for the treatment of leukemias caused by oncogenic PTKs. Proc Natl Acad Sci U S A. 2004; 101(9):3130-3135.
18. Jagani Z, Singh A, Khosravi-Far R. FoxO tumor suppressors and BCR-ABL-induced leukemia: a matter of evasion of apoptosis. Biochim Biophys Acta. 2008;1785(1):63-84.
19. Ghaffari S, Jagani Z, Kitidis C, Lodish HF, Khosravi-Far R. Cytokines and BCR-ABL mediate suppression of TRAIL-induced apoptosis through inhibition of forkhead FOXO3a transcription factor. Proc Natl Acad Sci U S A. 2003; 100(11):6523-6528.
20. Ye D, Wolff N, Li L, Zhang S, Ilaria RL Jr. STAT5 signaling is required for the efficient induction and maintenance of CML in mice. Blood. 2006; 107(12):4917-4925.
21. Hoelbl A, Schuster C, Kovacic B, et al. Stat5 is indispensable for the maintenance of bcr/ablpositive leukaemia. EMBO Mol Med. 2010;2(3): 98-110.
22. Warsch W, Kollmann K, Eckelhart E, et al. High STAT5 levels mediate imatinib resistance and indicate disease progression in chronic myeloid leukemia. Blood. 2011;117(12):3409-3420.
23. 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 U S A. 1999;96(22):12804-12809.
24. Holyoake TL, Jiang X, DrummondMW, Eaves AC, Eaves CJ. Elucidating critical mechanisms of deregulated stem cell turnover in the chronic phase of chronic myeloid leukemia. Leukemia. 2002; 16(4):549-558.
25. Perrotti D, Jamieson C, Goldman J, Skorski T. Chronic myeloid leukemia: mechanisms of blastic transformation. J Clin Invest. 2010;120(7):2254-2264.
26. Deininger M, Buchdunger E, Druker BJ. The development of imatinib as a therapeutic agent for chronic myeloid leukemia. Blood. 2005;105(7): 2640-2653.
27. O'Hare T, Eide CA, Deininger MW. Bcr-Abl kinase domain mutations, drug resistance, and the road to a cure for chronic myeloid leukemia. Blood. 2007;110(7):2242-2249.
28. Corbin AS, Buchdunger E, Pascal F, Druker BJ. Analysis of the structural basis of specificity of inhibition of the Abl kinase by STI571. J Biol Chem. 2002;277(35):32214-32219.
29. Lombardo LJ, Lee FY, Chen P, et al. Discovery of N-(2-chloro-6-methyl- phenyl)-2-(6-(4-(2- hydroxyethyl)-iperazin-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(27):6658-6661.
30. Talpaz M, Shah NP, Kantarjian H, et al. Dasatinib in imatinib-resistant Philadelphia chromosomepositive leukemias. N Engl J Med. 2006;354(24): 2531-2541.
31. Kantarjian H, Giles F, Wunderle L, et al. Nilotinib in imatinib-resistant CML and Philadelphia chromosome- positive ALL. N Engl J Med. 2006; 354(24):2542-2551.
32. Saglio G, Kim DW, Issaragrisil S, et al. Nilotinib versus imatinib for newly diagnosed chronic myeloid leukemia. N Engl J Med. 2010;362(24): 2251-2259.
33. Kantarjian H, Shah NP, Hochhaus A, et al. Dasatinib versus imatinib in newly diagnosed chronicphase chronic myeloid leukemia. N Engl J Med. 2010;362(24):2260-2270.
34. O'Hare T, Shakespeare WC, Zhu X, et al. AP24534, a pan-BCR-ABL inhibitor for chronic myeloid leukemia, potently inhibits the T315I mutant and overcomes mutation-based resistance. Cancer Cell. 2009;16(5):401-412.
35. O'Hare T, Deininger MW, Eide CA, Clackson T, Druker BJ. Targeting the BCR-ABL signaling pathway in therapy-resistant Philadelphia chromosome- positive leukemia. Clin Cancer Res. 2011;17(2):212-221.
36. Chan WW, Wise SC, Kaufman MD, et al. Conformational control inhibition of the BCR-ABL1 tyrosine kinase, including the gatekeeper T315I mutant, by the switch-control inhibitor DCC-2036. Cancer Cell. 2011;19(4):556-568.
37. Eide CA, Adrian LT, Tyner JW, et al. The ABL switch control inhibitor DCC-2036 is active against the chronic myeloid leukemia mutant BCR-ABLT315I and exhibits a narrow resistance profile. Cancer Res. 2011.
38. Preudhomme C, Guilhot J, Nicolini FE, et al. Imatinib plus peginterferon alfa-2a in chronic myeloid leukemia. N Engl J Med. 2010;363(26):2511-2521.
39. ClinicalTrials.gov. http://www.clinicaltrials.gov/ct2/ home. Accessed April 14, 2011.
40. Ross DM, Branford S, Seymour JF, et al. Patients with chronic myeloid leukemia who maintain a complete molecular response after stopping imatinib treatment have evidence of persistent leukemia by DNA PCR. Leukemia. 2010;24(10):1719-1724.
41. Sobrinho-Simoes M, Wilczek V, Score J, Cross NC, Apperley JF, Melo JV. In search of the original leukemic clone in chronic myeloid leukemia patients in complete molecular remission after stem cell transplantation or imatinib. Blood. 2010; 116(8):1329-1335.
42. Bhatia R, Holtz M, Niu N, et al. Persistence of malignant hematopoietic progenitors in chronic myelogenous leukemia patients in complete cytogenetic remission following imatinib mesylate treatment. Blood. 2003;101(12):4701-4707.
43. Graham SM, Jorgensen 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(1): 319-325.
44. + CML cells. Blood. 2007;109(9):4016-4019.
45. Konig H, Holyoake TL, Bhatia R. Effective and selective inhibition of chronic myeloid leukemia primitive hematopoietic progenitors by the dual Src/Abl kinase inhibitor SKI-606. Blood. 2008; 111(4):2329-2338.
46. 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(11):4532-4539.
47. Mahon FX, Rea 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(11):1029-1035.
48. Corbin AS, Agarwal A, Loriaux M, Cortes J, Deininger MW, Druker BJ. Human chronic myeloid leukemia stem cells are insensitive to imatinib despite inhibition of BCR-ABL activity. J Clin Invest. 2011;121:396-409.
49. 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(5):1109-1123.
50. Salomoni P, Calabretta B. Targeted therapies and autophagy: new insights from chronic myeloid leukemia. Autophagy. 2009;5(7):1050-1051.
51. Mizushima N. Autophagy: process and function. Genes Dev. 2007;21(22):2861-2873.
52. Levine B, Klionsky DJ. Development by selfdigestion: molecular mechanisms and biological functions of autophagy. Dev Cell. 2004;6(4):463-477.
53. Jung CH, Jun CB, Ro SH, et al. ULK-Atg13- FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell. 2009; 20(7):1992-2003.
54. Egan DF, Shackelford DB, Mihaylova MM, et al. Phosphorylation of ULK1 (hATG1) by AMPactivated protein kinase connects energy sensing to mitophagy. Science. 2011;331(6016):456-461.
55. Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011;13(2):132-141.
56. Hosokawa N, Hara T, Kaizuka T, et al. Nutrientdependent mTORC1 association with the ULK1- Atg13-FIP200 complex required for autophagy. Mol Biol Cell. 2009;20(7):1981-1991.
57. Liang C, Lee JS, Inn KS, et al. Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat Cell Biol. 2008;10(7):776-787.
58. Maiuri MC, Le Toumelin G, Criollo A, et al. Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J. 2007;26(10):2527-2539.
59. Pattingre S, Tassa A, Qu X, et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell. 2005;122(6):927-939.
60. Hoyer-Hansen M, Bastholm L, Szyniarowski P, et al. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol Cell. 2007;25(2):193-205.
61. Liang C, Feng P, Ku B, et al. Autophagic and tumour suppressor activity of a novel Beclin1- binding protein UVRAG. Nat Cell Biol. 2006;8(7): 688-699.
62. Ohsumi Y. Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol. 2001;2(3):211-216.
63. Geng J, Klionsky DJ. The Atg8 and Atg12 ubiquitin- like conjugation systems in macroautophagy. 'Protein modifications: beyond the usual suspects' review series. EMBO Rep. 2008;9(9):859-864.
64. Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol. 2009;10(7):458-467.
65. Kabeya Y, Mizushima N, Ueno T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 2000;19(21):5720-5728.
66. Klionsky DJ, Abeliovich H, Agostinis P, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy. 2008;4(2):151-175.
67. Eskelinen EL. Maturation of autophagic vacuoles in Mammalian cells. Autophagy. 2005;1(1):1-10.
68. Xie Z, Klionsky DJ. Autophagosome formation: core machinery and adaptations. Nat Cell Biol. 2007;9(10):1102-1109.
69. Rosenfeldt MT, Ryan KM. The multiple roles of autophagy in cancer. Carcinogenesis. 2011; 32(7):955-963.
70. Rubinsztein DC, Gestwicki JE, Murphy LO, Klionsky DJ. Potential therapeutic applications of autophagy. Nat Rev Drug Discov. 2007;6(4):304-312.
71. Liang XH, Jackson S, Seaman M, et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature. 1999;402(6762):672-676.
72. Yue Z, Jin S, Yang C, Levine AJ, Heintz N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci U S A. 2003;100(25): 15077-15082.
73. Degenhardt K, Mathew R, Beaudoin B, et al. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell. 2006;10(1):51-64.
74. Yamamoto A, Tagawa Y, Yoshimori T, Moriyama Y, Masaki R, Tashiro Y. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct. 1998;23(1):33-42.
75. Altman BJ, Jacobs SR, Mason EF, et al. Autophagy is essential to suppress cell stress and to allow BCR-Abl-mediated leukemogenesis. Oncogene. 2011;30(16):1855-1867.
76. Liu F, Guan JL. FIP200, an essential component of mammalian autophagy is indispensible for fetal hematopoiesis. Autophagy. 2011;7(2):229-230.
77. Mortensen M, Soilleux EJ, Djordjevic G, et al. The autophagy protein Atg7 is essential for hematopoietic stem cell maintenance. J Exp Med. 2011; 208(3):455-467.
78. Calabretta B, Salomoni P. Inhibition of autophagy: a new strategy to enhance sensitivity of chronic myeloid leukemia stem cells to tyrosine kinase inhibitors. Leuk Lymphoma. 2011;52(suppl 1):54-59.
79. Amaravadi RK, Yu D, Lum JJ, et al. Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J Clin Invest. 2007;117(2):326-336.
80. Yan CH, Liang ZQ, Gu ZL, Yang YP, Reid P, Qin ZH. Contributions of autophagic and apoptotic mechanisms to CrTX-induced death of K562 cells. Toxicon. 2006;47(5):521-530.
81. Carew JS, Nawrocki ST, Kahue CN, et al. Targeting autophagy augments the anticancer activity of the histone deacetylase inhibitor SAHA to overcome Bcr-Abl-mediated drug resistance. Blood. 2007;110(1):313-322.
82. Carew JS, Nawrocki ST, Giles FJ, Cleveland JL. Targeting autophagy: a novel anticancer strategy with therapeutic implications for imatinib resistance. Biologics. 2008;2(2):201-204.
83. Kamitsuji Y, Kuroda J, Kimura S, et al. The Bcr-Abl kinase inhibitor INNO-406 induces autophagy and different modes of cell death execution in Bcr-Abl-positive leukemias. Cell Death Differ. 2008;15(11):1712-1722.
84. Mishima Y, Terui Y, Taniyama A, et al. Autophagy and autophagic cell death are next targets for elimination of the resistance to tyrosine kinase inhibitors. Cancer Sci. 2008;99(11):2200-2208.
85. Crowley LC, Elzinga BM, O'Sullivan GC, McKenna SL. Autophagy induction by Bcr- Abl-expressing cells facilitates their recovery from a targeted or nontargeted treatment. Am J Hematol. 2011;86(1):38-47.
86. Carayol N, Vakana E, Sassano A, et al. Critical roles for mTORC2- and rapamycin-insensitive mTORC1-complexes in growth and survival of BCR-ABL-expressing leukemic cells. Proc Natl Acad Sci U S A. 2010;107(28):12469-12474.
87. Puissant A, Robert G, Fenouille N, et al. Resveratrol promotes autophagic cell death in chronic myelogenous leukemia cells via JNK-mediated p62/SQSTM1 expression and AMPK activation. Cancer Res. 2010;70(3):1042-1052.
88. Yogalingam G, Pendergast AM. Abl kinases regulate autophagy by promoting the trafficking and function of lysosomal components. J Biol Chem. 2008;283(51):35941-35953.
89. Altman BJ, Jacobs SR, Mason EF, et al. Autophagy is essential to suppress cell stress and to allow BCR-Abl-mediated leukemogenesis. Oncogene. 2010.
90. White E, DiPaola RS. The double-edged sword of autophagy modulation in cancer. Clin Cancer Res. 2009;15(17):5308-5316.
91. Chen S, Rehman SK, Zhang W, Wen A, Yao L, Zhang J. Autophagy is a therapeutic target in anticancer drug resistance. Biochim Biophys Acta. 2010;1806(2):220-229.