Identification of mcl-1 as a BCR/ABL-dependent target in chronic myeloid leukemia (CML): Evidence for cooperative antileukemic effects of imatinib and mcl-1 antisense oligonucleotides

Blood

Volumn 105, Issue 8, 2005, Pages 3303-3311

  Alchberger, Karl J ^b   Mayerhofer, Matthias ^b   Krauth, Maria Theresa ^b   Skvara, Hans ^b   Florian, Stefan ^b   Sonneck, Karoline ^b   Akgul, Cahit ^b   Derdak, Sophia ^b   Pickl, Winfried F ^b   Wacheck, Volker ^b   Selzer, Edgar ^b   Monia, Brett P ^b   Moriggl, Richard ^b   Valent, Peter ^b   Sillaber, Christian ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; ANTILEUKEMIC AGENT; ANTINEOPLASTIC AGENT; ANTISENSE OLIGONUCLEOTIDE; BCR ABL PROTEIN; IMATINIB; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN MCL 1; RAPAMYCIN; SMALL INTERFERING RNA;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER SURVIVAL; CELL ISOLATION; CELL SURVIVAL; CELL VIABILITY; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; DRUG MECHANISM; DRUG TARGETING; ENZYME INHIBITION; GROWTH INHIBITION; HUMAN; HUMAN CELL; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DETERMINATION; PROTEIN EXPRESSION;

EID: 20144388297     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2004-02-0749     Document Type: Article

References (69)

1. Nowell PC, Hungerford DA. A minute chromosome in human granulocytic leukemia. Science. 1960;132:1497-1499.
2. Rowley JD. A new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature. 1973;243:290-293.
3. de Klein A, van Kessel AG, Grosveld G, et al. A cellular oncogene is translocated to the Philadelphia chromosome in chronic myelocytic leukaemia. Nature. 1982;300:765-767.
4. 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;75:175-185.
5. Skorski T, Bellacosa A, Nieborowska-Skorska M. et al. Transformation of hematopoietic cells by BCR/ABL requires activation of a PI-3k/Akt-dependent pathway. EMBO J. 1997;16:6151-6161.
6. Sillaber C, Gesbert F, Frank DA, Sattler M, Griffin JD. STAT5 activation contributes to growth and viability in Bcr/Abl-transformed cells. Blood. 2000; 95:2118-2125.
7. Nieborowska-Skorska M, Wasik MA, Slupianek A, et al. Signal transducer and activator of transcription (STAT)5 activation by BCR/ABL is dependent on intact Src homology (SH)S and SH2 domains of BCR/ABL and is required for leukemogenesis. J Exp Med. 1999;189:1229-1242.
8. Puil L, Liu J, Gish G, et al. Bcr-Abl oncoproteins bind directly to activators of the Ras signalling pathway. EMBO J. 1994;13:764-773.
9. 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 USA. 1988;85:9312-9316.
10. Bedi A, Zehnbauer BA, Barber JP, Sharkis SJ, Jones RJ. Inhibition of apoptosis by BCR-ABL in chronic myeloid leukemia. Blood. 1994;83:2038-2044.
11. Deininger MW, Goldman JM, Melo JV. The molecular biology of chronic myeloid leukemia. Blood. 2000;96:3343-3356.
12. 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 USA. 1999;96:12804-12809.
13. Amarante-Mendes GP, McGahon AJ, Nishioka WK, Afar DE, Witte ON, Green DR. Bcl-2-independent Bcr-Abl-mediated resistance to apoptosis: protection is correlated with up regulation of Bcl-xL. Oncogene. 1998;16:1383-1390.
14. Gesbert F, Griffin JD. Bcr/Abl activates transcription of the Bcl-X gene through STAT5. Blood. 2000;96:2269-2276.
15. Horita M, Andreu EJ, Benito A, et al. Blockade of the Bcr-Abl kinase activity induces apoptosis of chronic myelogenous leukemia cells by suppressing signal transducer and activator of transcription 5-dependent expression of Bcl-xL. J Exp Med. 2000;191:977-984.
16. Nieborowska-Skorska M, Hoser G, Kossev P, Wasik MA, Skorski T. Complementary functions of the antiapoptotic protein A1 and serine/threonine kinase pim-1 in the BCR/ABL-mediated leukemogenesis. Blood. 2002;99:4531-4539.
17. Ravandi F, Kantarjian HM, Talpaz M, et al. Expression of apoptosis proteins in chronic myelogenous leukemia: associations and significance. Cancer. 2001;91:1964-1972.
18. Kozopas KM, Yang T, Buchan HL, Zhou P, Craig RW. MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL2. Proc Natl Acad Sci USA. 1993;90:3516-3520.
19. Fukuchi Y, Kizaki M, Yamato K, et al. Mcl-1, an early-induction molecule, modulates activin A-induced apoptosis and differentiation of CML cells. Oncogene. 2001;20:704-713.
20. Zhou P, Qian L, Kozopas KM, Craig RW. Mcl-1, a Bcl-2 family member, delays the death of hematopoletic cells under a variety of apoptosis-inducing conditions. Blood. 1997;89:630-643.
21. Zhan Q, Bieszczad CK, Bae I, Fornace AJ Jr, Craig RW. Induction of BCL2 family member MCL1 as an early response to DNA damage. Oncogene. 1997;14:1031-1039.
22. Yu C, Krystal G, Varticovksi L, et al. Pharmacologic mitogen-activated protein/extracellular signal-regulated kinase kinase/mitogen-activated protein kinase inhibitors interact synergistically with STI571 to induce apoptosis in Bcr/Abl-expressing human leukemia cells. Cancer Res. 2002;62:188-199.
23. + human myeloid leukemia cells. Cancer Res. 2003;63:2118-2126.
24. Fasano O, Taparowsky E, Fiddes J, Wigler M, Goldfarb M. Sequence and structure of the coding region of the human H-ras-1 gene from T24 bladder carcinoma cells. J Mol Appl Genet. 1983;2:173-180.
25. Vojtek AB, Hollenberg SM, Cooper JA. Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell. 1993;74:205-214.
26. Feig LA, Cooper GM. Inhibition of NIH 3T3 cell proliferation by a mutant ras protein with preferential affinity for GDP. Mol Cell Biol. 1988;8:3235-3243.
27. Sedlak TW, Oltvai ZN, Yang E, et al. Multiple Bcl-2 family members demonstrate selective dimerizations with Bax. Proc Natl Acad Sci USA. 1995;92:7834-7838.
28. Yang E, Zha J, Jockel J, Boise LH, Thompson CB, Korsmeyer SJ. Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell. 1995;80:285-291.
29. Akgul C, Turner PC, White MR, Edwards SW. Functional analysis of the human MCL-1 gene. Cell Mol Life Sci. 2000;57:684-691.
30. Mayerhofer M, Valent P, Sperr WR, Griffin JD, Sillaber C. BCR/ABL induces expression of vascular endothelial growth factor and its transcriptional activator, hypoxia inducible factor, through a pathway involving phosphoinositide 3-kinase and the mammalian target of rapamycin. Blood. 2002;100:3767-3775.
31. Weisberg E, Griffin JD. Mechanism of resistance to the ABL tyrosine kinase inhibitor STI571 in BCR/ABL-transformed hematopoietic cell lines. Blood. 2000;95:3498-3505.
32. Chomczynski P. One-hour downward alkaline capillary transfer for blotting of DNA and RNA. Anal Biochem. 1992;201:134-139.
33. Mayerhofer M, Florian S, Krauth MT, et al. Identification of Heme oxygenase-1 as a novel BCR/ ABL-dependent survival factor in chronic myeloid leukemia. Cancer Res. 2004;64:3148-3154.
34. Thallinger C, Wolschek MF, Wacheck V, et al. Mcl-1 antisense therapy chemosensitizes human melanoma in a SCID mouse xenotransplantation model. J Invest Dermatol. 2003;120:1081-1086.
35. Nijhawan D, Fang M, Traer E, et al. Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation. Genes Dev. 2003;17:1475-1486.
36. Van Cruchten S, van Den S, Broeck W. Morphological and biochemical aspects of apoptosis, oncosis and necrosis. Anat Histol Embryol. 2002;31:214-223.
37. Moriggl R, Gouilleux-Gruart V, Jahne R, et al. Deletion of the carboxyl-terminal transactivation domain of MGF-Stat5 results in sustained DNA binding and a dominant negative phenotype. Mol Cell Biol. 1996;16:5691-5700.
38. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul. 1984;22:27-55.
39. Berenbaum MC. What is synergy? Pharmacol Rev. 1989;41:93-141.
40. Druker BJ, Tamura S, Buchdunger E, et al. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of BCR-ABL positive cells. Nat Med. 1996;2:561-566.
41. Druker BJ, Talpaz M, Resta DJ, et al. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med. 2001;344:1031-1037.
42. O'Brien SG, Guilhot F, Larson RA, et al. Imatinib compared with interferon and low-dose cytarabine for newly diagnosed chronic-phase chronic myeloid leukemia. N Engl J Med. 2003;348:994-1004.
43. Gorre ME, Sawyers CL Molecular mechanisms of resistance to STI571 in chronic myeloid leukemia. Curr Opin Hematol. 2002;9:303-307.
44. Gorre ME, Mohammed M, Ellwood K, et al. Clinical resistance to STI-571 cancer therapy caused by BCR/ABL gene mutation or amplification. Science. 2001;293:876-880.
45. Hochhaus A, Kreil S, Corbin A, et al. Roots of clinical resistance to STI-571 cancer therapy. Science. 2001;293:2163.
46. Hochhaus A, Kreil S, Corbin AS, et al. Molecular and chromosomal mechanisms of resistance to imatinib (STI571) therapy. Leukemia. 2002;16:2190-2196.
47. Selzer E, Thallinger C, Hoeller C, et al. Betulinic acid-induced Mcl-1 expression in human melanoma-mode of action and functional significance. Mol Med. 2002;8:877-884.
48. Derenne S, Monia B, Dean NM, et al. Antisense strategy shows that Mcl-1 rather than Bcl-2 or Bcl-xL is an essential survival protein of human myeloma cells. Blood. 2002;100:194-199.
49. Mow BM, Chandra J, Svingen PA, et al. Effects of the Bcr/abl kinase inhibitors STI571 and adaphostin (NSC 680410) on chronic myelogenous leukemia cells in vitro. Blood. 2002;99:664-671.
50. Wang JM, Lai MZ, Yang-Yen HF. Interleukin-3 stimulation of mcl-1 gene transcription involves activation of the PU. 1 transcription factor through a p38 mitogen-activated protein kinase-dependent pathway. Mol Cell Biol. 2003;23:1896-1909.
51. Wang JM, Chao JR, Chen W, Kuo ML, Yen JJ, Yang-Yen HF. The antiapoptotic gene mcl-1 is up-regulated by the phosphatidylinositol 3-kinase/ Akt signaling pathway through a transcription factor complex containing CREB. Mol Cell Biol. 1999;19:6195-6202.
52. Chao JR, Wang JM, Lee SF, et al. mcl-1 is an immediate-early gene activated by the granulocyte-macrophage colony-stimulating factor (GM-CSF) signaling pathway and is one component of the GM-CSF viability response. Mol Cell Biol. 1998;18:4883-4898.
53. Schubert KM, Duronio V. Distinct roles for extracellular-signal-regulated protein kinase (ERK) mitogen-activated protein kinases and phosphatidylinositol 3-kinase in the regulation of Mcl-1 synthesis. Biochem J. 2001;356:473-480.
54. Sattler M, Griffin JD. Molecular mechanisms of transformation by the BCR-ABL oncogene. Semin Hematol. 2003;40:4-10.
55. Testa U, Riccioni R, Militi S, et al. Elevated expression of IL-3Ralpha in acute myelogenous leukemia is associated with enhanced blast proliferation, increased cellularity, and poor prognosis. Blood. 2002;100:2980-2988.
56. Townsend KJ, Trusty JL, Traupman MA, Eastman A, Craig RW. Expression of the antiapoptotic MCL1 gene product is regulated by a mitogen activated protein kinase-mediated pathway triggered through microtubule disruption and protein kinase C. Oncogene. 1998;17:1223-1234.
57. Huang HM, Huang CJ, Yen JJ. Mcl-1 is a common target of stem cell factor and interleukin-5 for apoptosis prevention activity via MEK/MAPK and PI-3K/Akt pathways. Blood. 2000;96:1764-1771.
58. Huang M, Dorsey JF, Epling-Burnette PK, et al. Inhibition of Bcr-Abl kinase activity by PD180970 blocks constitutive activation of Stat5 and growth of CMLcells. Oncogene. 2002;21:8804-8816.
59. Buettner R, Mora LB, Jove R. Activated STAT signaling in human tumors provides novel molecular targets for therapeutic intervention. Clin Cancer Res. 2002;8:945-954.
60. Craig RW. MCL1 provides a window on the role of the BCL2 family in cell proliferation, differentiation and tumorigenesis. Leukemia. 2002;16:444-454.
61. Hoover RR, Gerlach MJ, Koh EY, Daley GQ. Cooperative and redundant effects of STAT5 and Ras signaling in BCR/ABL transformed hematopoietic cells. Oncogene. 2001;20:5826-5835.
62. Sonoyama J, Matsumura I, Ezoe S, et al. Functional cooperation among Ras, STAT5, and phosphatidylinositol 3-kinase is required for full oncogenic activities of BCR/ABL in K562 cells. J Biol Chem. 2002;277:8076-8082.
63. Cowan-Jacob SW, Guez V, Fendrich G, et al. Imatinib (STI571) resistance in chronic myelogenous leukemia: molecular basis of the underlying mechanisms and potential strategies for treatment. Mini Rev Med Chem. 2004;4:285-299.
64. Weisberg E, Griffin JD. Resistance to imatinib (Glivec): update on clinical mechanisms. Drug Resist Updat. 2003;6:231-238.
65. La Rosee P, O'Dwyer ME, Druker BJ. Insights from pre-cllnical studies for new combination treatment regimens with the Bcr-Abl kinase inhibitor imatinib mesylate (Gleevec/Glivec) in chronic myelogenous leukemia: a translational perspective. Leukemia. 2002;16:1213-1219.
66. Sillaber C, Mayerhofer M, Agis H, et al. Chronic myeloid leukemia: pathophysiology, diagnostic parameters, and current treatment concepts. Wien Klin Wochenschr. 2003;115:485-504.
67. Moulding DA, Giles RV, Spiller DG, White MR, Tidd DM, Edwards SW. Apoptosis is rapidly triggered by antisense depletion of MCL-1 in differentiating U937 cells. Blood. 2000;96:1756-1763.
68. Biroccio A, Leonetti C, Zupi G. The future of antisense therapy: combination with anticancer treatments. Oncogene. 2003;22:6579-6588.
69. Jansen B, Zangemeister-Wittke U. Antisense therapy for cancer - the time of truth. Lancet Oncol. 2002;3:672-683.