Critical roles for mTORC2- and rapamycin-insensitive mTORC1-complexes in growth and survival of BCR-ABL-expressing leukemic cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 28, 2010, Pages 12469-12474

  Carayol, Nathalie ^a   Vakana, Eliza ^a   Sassano, Antonella ^a   Kaur, Surinder ^a   Goussetis, Dennis J ^a   Glaser, Heather ^a   Druker, Brian J ^b   Donato, Nicholas J ^c   Altman, Jessica K ^a   Barr, Sharon ^d   Platanias, Leonidas C ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c UNIVERSITY OF MICHIGAN COMPREHENSIVE CANCER CENTER   (United States)

^d OSI PHARMACEUTICALS INC   (United States)

Author keywords

Cell proliferation; Cellular signaling; Kinase; mRNA translation; OSI 027

Indexed keywords

BCR ABL PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; OSI 027; RAPAMYCIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER GROWTH; CELL SURVIVAL; HUMAN; HUMAN CELL; LEUKEMIA CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

APOPTOSIS; CELLULAR STRUCTURES; FUSION PROTEINS, BCR-ABL; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MUTATION; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; SIROLIMUS;

EID: 77955443001     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1005114107     Document Type: Article

References (51)

1. Sherbenou DW, Druker BJ (2007) Applying the discovery of the Philadelphia chromosome. J Clin Invest 117:2067-2074.
2. Druker BJ (2008) Translation of the Philadelphia chromosome into therapy for CML. Blood 112:4808-4817.
3. Groffen J, et al. (1984) Philadelphia chromosomal breakpoints are clustered within a limited region, bcr, on chromosome 22. Cell 36:93-99. (Pubitemid 14155374)
4. Heisterkamp N, Stam K, Groffen J, de Klein A, Grosveld G (1985) Structural organization of the bcr gene and its role in the Ph' translocation. Nature 315:758-761. (Pubitemid 15022931)
5. Ben-Neriah Y, Daley GQ, Mes-Masson AM, Witte ON, Baltimore D (1986) The chronic myelogenous leukemia-specific P210 protein is the product of the bcr/abl hybrid gene. Science 233:212-214. (Pubitemid 16008117)
6. Daley GQ, Van Etten RA, Baltimore D (1990) Induction of chronic myelogenous leukemia in mice by the P210bcr/abl gene of the Philadelphia chromosome. Science 247:824-830. (Pubitemid 120031362)
7. Lugo TG, Pendergast AM, Muller AJ, Witte ON (1990) Tyrosine kinase activity and transformation potency of bcr-abl oncogene products. Science 247:1079-1082.
8. Mauro MJ, O'Dwyer M, Heinrich MC, Druker BJ (2002) STI571: A paradigm of new agents for cancer therapeutics. J Clin Oncol 20:325-334. (Pubitemid 34032628)
9. Deininger M, Buchdunger E, Druker BJ (2005) The development of imatinib as a therapeutic agent for chronic myeloid leukemia. Blood 105:2640-2653.
10. O'Hare T, et al. (2005) In vitro activity of Bcr-Abl inhibitors AMN107 and BMS-354825 aga inst clinically relevant imatinib-resistant Abl kinase domain mutants. Cancer Res 65:4500-4505.
11. Shah NP, et al. (2004) Overriding imatinib resistance with a novel ABL kinase inhibitor. Science 305:399-401.
12. Hochhaus A, et al. (2007) Dasatinib induces notable hematologic and cytogenetic responses in chronic-phase chronic myeloid leukemia after failure of imatinib therapy. Blood 109:2303-2309. (Pubitemid 46425867)
13. Kantarjian H, Jabbour E, Grimley J, Kirkpatrick P (2006) Dasatinib. Nat Rev Drug Discov 5:717-718.
14. Ray A, Cowan-Jacob SW, Manley PW, Mestan J, Griffin JD (2007) Identification of BCR-ABL point mutations conferring resistance to the Abl kinase inhibitor AMN107 (nilotinib) by a random mutagenesis study. Blood 109:5011-5015.
15. von Bubnoff N, et al. (2006) Bcr-Abl resistance screening predicts a limited spectrum of point mutations to be associated with clinical resistance to the Abl kinase inhibitor nilotinib (AMN107). Blood 108:1328-1333.
16. Fabbro D, et al. (2010) Inhibitors of the Abl kinase directed at either the ATP-or myristate-binding site. Biochim Biophys Acta 1804:454-462.
17. Zhang J, et al. (2010) Targeting Bcr-Abl by combining allosteric with ATP-binding-site inhibitors. Nature 463:501-506.
18. Donato NJ, et al. (2003) BCR-ABL independence and LYN kinase overexpression in chronic myelogenous leukemia cells selected for resistance to STI571. Blood 101:690-698.
19. Dai Y, Rahmani M, Corey SJ, Dent P, Grant S (2004) A Bcr/Abl-independent, Lyn-dependent form of imatinib mesylate (STI-571) resistance is associated with altered expression of Bcl-2. J Biol Chem 279:34227-34239. (Pubitemid 39318046)
20. Hu Y, et al. (2004) Requirement of Src kinases Lyn, Hck and Fgr for BCR-ABL1-induced B-lymphoblastic leukemia but not chronic myeloid leukemia. Nat Genet 36:453-461.
21. Bjornsti MA, Houghton PJ (2004) The TOR pathway: A target for cancer therapy. Nat Rev Cancer 4:335-348. (Pubitemid 38579480)
22. Guertin DA, Sabatini DM (2007) Defining the role of mTOR in cancer. Cancer Cell 12:9-22.
23. Bhagwat SV, et al. (2010) OSI-027, a potent and selective small molecule mTORC1/mTORC2 kinase Inhibitor is mechanistically distinct from rapamycin. P Am Assoc Canc Res (Abstract 4487).
24. Ly C, Arechiga AF, Melo JV, Walsh CM, Ong ST (2003) Bcr-Abl kinase modulates the translation regulators ribosomal protein S6 and 4E-BP1 in chronic myelogenous leukemia cells via the mammalian target of rapamycin. Cancer Res 63:5716-5722. (Pubitemid 37187466)
25. Mohi MG, et al. (2004) Combination of rapamycin and protein tyrosine kinase (PTK) inhibitors for the treatment of leukemias caused by oncogenic PTKs. Proc Natl Acad Sci USA 101:3130-3135.
26. Parmar S, et al. (2005) Differential regulation of the p70 S6 kinase pathway by interferon alpha (IFNalpha) and imatinib mesylate (STI571) in chronic myelogenous leukemia cells. Blood 106:2436-2443.
27. Carayol N, et al. (2008) Suppression of programmed cell death 4 (PDCD4) protein expression by BCR-ABL-regulated engagement of the mTOR/p70 S6 kinase pathway. J Biol Chem 283:8601-8610.
28. Copp J, Manning G, Hunter T (2009) TORC-specific phosphorylation of mammalian target of rapamycin (mTOR): Phospho-Ser2481 is a marker for intact mTOR signaling complex 2. Cancer Res 69:1821-1827.
29. Platanias LC (2005) Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol 5:375-386.
30. Wu J, et al. (2010) ON012380, a putative BCR-ABL kinase inhibitor with a unique mechanism of action in imatinib-resistant cells. Leukemia 24:869-872.
31. Bellodi C, et al. (2009) Targeting autophagy potentiates tyrosine kinase inhibitor-induced cell death in Philadelphia chromosome-positive cells, including primary CML stem cells. J Clin Invest 119:1109-1123.
32. Salomoni P, Calabretta B (2009) Targeted therapies and autophagy: New insights from chronic myeloid leukemia. Autophagy 5:1050-1051.
33. Cecconi F, Levine B (2008) The role of autophagy in mammalian development: cell makeover rather than cell death. Dev Cell 15:344-357.
34. Druker BJ, et al. (2006) Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N Engl J Med 355:2408-2417. (Pubitemid 44903745)
35. Bixby D, Talpaz M (2009) Mechanisms of resistance to tyrosine kinase inhibitors in chronic myeloid leukemia and recent therapeutic strategies to overcome resistance. Hematology 1:461-476.
36. Redaelli S, et al. (2009) Activity of bosutinib, dasatinib, and nilotinib against 18 imatinib-resistant BCR/ABL mutants. J Clin Oncol 27:469-471.
37. Weisberg E, et al. (2005) Characterization of AMN107, a selective inhibitor of native and mutant Bcr-Abl. Cancer Cell 7:129-141. (Pubitemid 40248339)
38. Kantarjian H, et al. (2006) Nilotinib in imatinib-resistant CML and Philadelphia chromosome-positive ALL. N Engl J Med 354:2542-2551. (Pubitemid 43882350)
39. Talpaz M, et al. (2006) Dasatinib in imatinib-resistant Philadelphia chromosome-positive leukemias. N Engl J Med 354:2531-2541. (Pubitemid 43882349)
40. Hay N (2005) The Akt-mTOR tango and its relevance to cancer. Cancer Cell 8:179-183.
41. Altman JK, Platanias LC (2008) Exploiting the mammalian target of rapamycin pathway in hematologic malignancies. Curr Opin Hematol 15:88-94.
42. Kharas MG, Fruman DA (2005) ABL oncogenes and phosphoinositide 3-kinase: Mechanism of activation and downstream effectors. Cancer Res 65:2047-2053.
43. Prabhu S, et al. (2007) A novel mechanism for Bcr-Abl action: Bcr-Abl-mediated induction of the eIF4F translation initiation complex and mRNA translation. Oncogene 26:1188-1200. (Pubitemid 46310452)
44. Bhaskar PT, Hay N (2007) The two TORCs and Akt. Dev Cell 12:487-502.
45. Furic L, Livingstone M, Dowling RJ, Sonenberg N (2009) Targeting mTOR-dependent tumours with specific inhibitors: A model for personalized medicine based on molecular diagnoses. Curr Oncol 16:59-61.
46. Manning BD (2004) Balancing Akt with S6K: Implications for both metabolic diseases and tumorigenesis. J Cell Biol 167:399-403.
47. Janes MR, et al. (2010) Effective and selective targeting of leukemia cells using a TORC1/2 kinase inhibitor. Nat Med 16:205-213.
48. Kroczynska B, et al. (2009) Interferon-dependent engagement of eukaryotic initiation factor 4B via S6 kinase (S6K)- and ribosomal protein S6K-mediated signals. Mol Cell Biol 29:2865-2875.
49. Altman JK, et al. (2008) Regulatory effects of mammalian target of rapamycin-mediated signals in the generation of arsenic trioxide responses. J Biol Chem 283:1992-2001.
50. Kaur S, et al. (2008) Role of the Akt pathway in mRNA translation of interferon-stimulated genes. Proc Natl Acad Sci USA 105:4808-4813.
51. Jackson WT, et al. (2005) Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol 3:e156.