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PMID: 18385754 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Effective killing of Gleevec-resistant CML cells with T315I mutation by a natural compound PEITC through redox-mediated mechanism.

Leukemia ·Vol. 22 ·No. 6 ·2008-06-00 ·Pages 1191-9

Zhang H, Trachootham D, Lu W, Carew J, Giles FJ, Keating MJ, Arlinghaus RB, Huang P

Abstract

Mutation of Bcr-Abl is an important mechanism by which chronic myelogenous leukemia (CML) cells become resistant to Gleevec. The T315I mutation is clinically significant since CML cells harboring this mutation are insensitive to Gleevec and other Bcr-Abl-targeted drugs. Identification of new agents capable of effectively killing CML cells with T315I mutation would have important therapeutic implications in Gleevec-resistant CML. Here, we showed that beta-phenylethyl isothiocyanate (PEITC), a natural compound found in vegetables, is effective in killing CML cells expressing T315I BCR-ABL. Treatment of leukemia cell lines harboring wild-type or mutant Bcr-Abl with 10 microM PEITC resulted in an elevated ROS stress and a redox-mediated degradation of the BCR-ABL protein, leading to massive death of the leukemia cells. Antioxidant NAC attenuated the PEITC-induced oxidative stress in CML cells and prevented the degradation of BCR-ABL, caspase-3 activation and cell death. We further showed that the ROS-induced degradation of BCR-ABL was mediated partially by caspase-3 and the proteasome pathway. The ability of PEITC to effectively kill T315I-positive CML cells was further confirmed using primary leukemia cells isolated from CML patients. Our results suggest that PEITC is a promising compound capable of killing Gleevec-resistant CML cells through a ROS-mediated mechanism and warrants further investigations.

MeSH Terms
Aldehyde Dehydrogenase/antagonists & inhibitors Animals Anticarcinogenic Agents/pharmacology Antineoplastic Agents/pharmacology Antioxidants/pharmacology Apoptosis/drug effects Benzamides Caspase 3/metabolism Cells, Cultured Drug Resistance, Neoplasm Enzyme Activation/drug effects Fusion Proteins, bcr-abl/genetics,metabolism Glutathione/metabolism Humans Imatinib Mesylate Immunoblotting Isothiocyanates/therapeutic use Leukemia, Myelogenous, Chronic, BCR-ABL Positive/genetics,pathology Mice Mutation/genetics Oxidation-Reduction Piperazines/pharmacology Precursor Cells, B-Lymphoid/drug effects,metabolism Protein-Tyrosine Kinases/antagonists & inhibitors Pyrimidines/pharmacology Reactive Oxygen Species/metabolism
Chemicals
Anticarcinogenic Agents Antineoplastic Agents Antioxidants Benzamides Isothiocyanates Piperazines Pyrimidines Reactive Oxygen Species phenethyl isothiocyanate Imatinib Mesylate Aldehyde Dehydrogenase Protein-Tyrosine Kinases Fusion Proteins, bcr-abl Caspase 3 Glutathione
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Zhang H
Department of Molecular Pathology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Trachootham D
Lu W
Carew J
Giles F J
Keating M J
Arlinghaus R B
Huang P
References (37)
37 references, click to expand
  1. Biological properties and growth in SCID mice of a new myelogenous leukemia cell line (KBM-5) derived from chronic myelogenous leukemia cells in the blastic phase.
    Cancer Res. 1993 Aug 1;53(15):3603-10 PMID: 8339266
  2. Overriding imatinib resistance with a novel ABL kinase inhibitor.
    Science. 2004 Jul 16;305(5682):399-401 PMID: 15256671
  3. Activation of the PI3K/mTOR pathway by BCR-ABL contributes to increased production of reactive oxygen species.
    Blood. 2005 Feb 15;105(4):1717-23 PMID: 15486067
  4. Mutation in the ATP-binding pocket of the ABL kinase domain in an STI571-resistant BCR/ABL-positive cell line.
    Cancer Res. 2002 Nov 1;62(21):5995-8 PMID: 12414617
  5. Requirement of caspase-mediated cleavage of c-Abl during stress-induced apoptosis.
    Cell Death Differ. 2004 Mar;11(3):290-300 PMID: 14657961
  6. Vaccination with leukemia cells expressing cell-surface-associated GM-CSF blocks leukemia induction in immunocompetent mice.
    Oncogene. 2006 Jul 27;25(32):4483-90 PMID: 16547503
  7. Subcellular localization of Bcr, Abl, and Bcr-Abl proteins in normal and leukemic cells and correlation of expression with myeloid differentiation.
    J Clin Invest. 1993 Oct;92(4):1925-39 PMID: 8408645
  8. Caspase-dependent cleavage of c-Abl contributes to apoptosis.
    Mol Cell Biol. 2003 Apr;23(8):2790-9 PMID: 12665579
  9. High-performance liquid chromatography-based determination of total isothiocyanate levels in human plasma: application to studies with 2-phenethyl isothiocyanate.
    Anal Biochem. 2001 Apr 15;291(2):279-89 PMID: 11401302
  10. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia.
    N Engl J Med. 2001 Apr 5;344(14):1031-7 PMID: 11287972
  11. Effects of antioxidants and caspase-3 inhibitor on the phenylethyl isothiocyanate-induced apoptotic signaling pathways in human PLC/PRF/5 cells.
    Eur J Pharmacol. 2005 Aug 22;518(2-3):96-106 PMID: 16054126
  12. Expression of interferon consensus sequence binding protein induces potent immunity against BCR/ABL-induced leukemia.
    Blood. 2001 Jun 1;97(11):3491-7 PMID: 11369642
  13. Janus kinase 2: a critical target in chronic myelogenous leukemia.
    Cancer Res. 2006 Jul 1;66(13):6468-72 PMID: 16818614
  14. Flying under the radar: the new wave of BCR-ABL inhibitors.
    Nat Rev Drug Discov. 2007 Oct;6(10):834-48 PMID: 17853901
  15. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification.
    Science. 2001 Aug 3;293(5531):876-80 PMID: 11423618
  16. Chronic myeloid leukaemia as a model of disease evolution in human cancer.
    Nat Rev Cancer. 2007 Jun;7(6):441-53 PMID: 17522713
  17. Dasatinib induces complete hematologic and cytogenetic responses in patients with imatinib-resistant or -intolerant chronic myeloid leukemia in blast crisis.
    Blood. 2007 Apr 15;109(8):3207-13 PMID: 17185463
  18. Multiple BCR-ABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (STI571) in chronic phase and blast crisis chronic myeloid leukemia.
    Cancer Cell. 2002 Aug;2(2):117-25 PMID: 12204532
  19. The biology of chronic myeloid leukemia.
    N Engl J Med. 1999 Jul 15;341(3):164-72 PMID: 10403855
  20. Action of (E)-2'-deoxy-2'-(fluoromethylene)cytidine on DNA metabolism: incorporation, excision, and cellular response.
    Mol Pharmacol. 2002 Jan;61(1):222-9 PMID: 11752224
  21. Hematologic and cytogenetic responses to imatinib mesylate in chronic myelogenous leukemia.
    N Engl J Med. 2002 Feb 28;346(9):645-52 PMID: 11870241
  22. Mechanisms of BCR-ABL in the pathogenesis of chronic myelogenous leukaemia.
    Nat Rev Cancer. 2005 Mar;5(3):172-83 PMID: 15719031
  23. Synergistic effect of targeting mTOR by rapamycin and depleting ATP by inhibition of glycolysis in lymphoma and leukemia cells.
    Leukemia. 2005 Dec;19(12):2153-8 PMID: 16193082
  24. 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 Jul 1;102(1):276-83 PMID: 12623848
  25. BCR/ABL kinase induces self-mutagenesis via reactive oxygen species to encode imatinib resistance.
    Blood. 2006 Jul 1;108(1):319-27 PMID: 16527898
  26. Differential response of MG132 cytotoxicity against small cell lung cancer cells to changes in cellular GSH contents.
    Biochem Pharmacol. 2004 Aug 15;68(4):659-66 PMID: 15276073
  27. Up-regulation of c-Jun inhibits proliferation and induces apoptosis via caspase-triggered c-Abl cleavage in human multiple myeloma.
    Cancer Res. 2007 Feb 15;67(4):1680-8 PMID: 17308109
  28. Comparison of imatinib mesylate, dasatinib (BMS-354825), and nilotinib (AMN107) in an N-ethyl-N-nitrosourea (ENU)-based mutagenesis screen: high efficacy of drug combinations.
    Blood. 2006 Oct 1;108(7):2332-8 PMID: 16772610
  29. Free radical stress in chronic lymphocytic leukemia cells and its role in cellular sensitivity to ROS-generating anticancer agents.
    Blood. 2003 May 15;101(10):4098-104 PMID: 12531810
  30. Circumventing resistance to kinase-inhibitor therapy.
    N Engl J Med. 2006 Jun 15;354(24):2594-6 PMID: 16775240
  31. p53 expression in K562 cells is associated with caspase-mediated cleavage of c-ABL and BCR-ABL protein kinases.
    Br J Haematol. 2002 Jun;117(3):588-97 PMID: 12028026
  32. N-acetyl-cysteine enhances growth in BCR-ABL-transformed cells.
    Cancer Sci. 2005 Apr;96(4):240-4 PMID: 15819723
  33. The BCR/ABL tyrosine kinase induces production of reactive oxygen species in hematopoietic cells.
    J Biol Chem. 2000 Aug 11;275(32):24273-8 PMID: 10833515
  34. The two major imatinib resistance mutations E255K and T315I enhance the activity of BCR/ABL fusion kinase.
    Biochem Biophys Res Commun. 2004 Jul 9;319(4):1272-5 PMID: 15194504
  35. Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by beta-phenylethyl isothiocyanate.
    Cancer Cell. 2006 Sep;10(3):241-52 PMID: 16959615
  36. Enhanced Bcr-Abl-specific antileukemic activity of arsenic trioxide (Trisenox) through glutathione-depletion in imatinib-resistant cells.
    Haematologica. 2007 Jun;92(6):838-41 PMID: 17550858
  37. Dasatinib in imatinib-resistant Philadelphia chromosome-positive leukemias.
    N Engl J Med. 2006 Jun 15;354(24):2531-41 PMID: 16775234
Article Info
Journal
Leukemia
Abbr.
Leukemia
ISSN
1476-5551
Published
2008-06-00
Epub
2008-00-03
Pages
1191-9
Language
English
Region
England
NLM ID
8704895
PMCID
PMC2585768
Subset
IM
Grants
NCI NIH HHS · R01 CA085563 · United States
NCI NIH HHS · CA16672 · United States
NCI NIH HHS · CA109041 · United States
NCI NIH HHS · R01 CA109041 · United States
NCI NIH HHS · CA100428 · United States
NCI NIH HHS · P30 CA016672-24S39021 · United States
NCI NIH HHS · CA085563 · United States
NCI NIH HHS · R01 CA100428 · United States
NCI NIH HHS · P30 CA016672 · United States
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