MDM2 antagonists induce p53-dependent apoptosis in AML: Implications for leukemia therapy

Blood

Volumn 106, Issue 9, 2005, Pages 3150-3159

  Kojima, Kensuke ^b   Konopleva, Marina ^b   Samudio, Ismael J ^b   Shikami, Masato ^b   Cabreira Hansen, Maria ^b   McQueen, Teresa ^b   Ruvolo, Vivian ^b   Tsao, Twee ^b   Zeng, Zhihong ^b   Vassilev, Lyubomir T ^b   Andreeff, Michael ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CASPASE; CD34 ANTIGEN; CYTARABINE; DNA FRAGMENT; DOXORUBICIN; MUTANT PROTEIN; NUTLIN 3A; PHOSPHATIDYLSERINE; PROTEIN BCL 2; PROTEIN INHIBITOR; PROTEIN MDM2; PROTEIN P53; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ADULT; AGED; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL MEMBRANE POTENTIAL; CELL PERMEABILIZATION; COLONY FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORRELATION ANALYSIS; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG MECHANISM; DRUG POTENTIATION; DRUG TARGETING; ENZYME ACTIVATION; FEMALE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MALE; MITOCHONDRIAL MEMBRANE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN TRANSPORT; STEM CELL; TRANSCRIPTION INITIATION; WILD TYPE;

EID: 27644568226     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2005-02-0553     Document Type: Article

References (60)

1. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature. 2000;408: 307-310.
2. Hollstein M, Sidransky D, Vogelstein B, Harris CC. p53 mutations in human cancers. Science. 1991;253:49-53.
3. Bykov VJ, Wiman KG. Novel cancer therapy by reactivation of the p53 apoptosis pathway. Ann Med. 2003;35:458-465.
4. Harris CC. Structure and function of the p53 tumor suppressor gene: clues for rational cancer therapeutic strategies. J Natl Cancer Inst. 1996;88:1442-1455.
5. Lowe SW, Ruley HE, Jacks T, Housman DE. p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell. 1993;74:957-967.
6. Roth JA, Grammer SF. Gene replacement therapy for non-small cell lung cancer: a review. Hematol Oncol Clin North Am. 2004;18:215-229.
7. Roth J, Lenz-Bauer C, Contente A, et al. Reactivation of mutant p53 by a one-hybrid adaptor protein. Cancer Res. 2003;63:3904-3908.
8. Hu G, Zhang W, Deisseroth AB. P53 gene mutations in acute myelogenous leukaemia. Br J Haematol. 1992;81:489-494.
9. Schottelius A, Brennscheidt U, Ludwig WD, Mertelsmann RH, Herrmann F, Lubbert M. Mechanisms of p53 alteration in acute leukemias. Leukemia. 1994;8:1673-1681.
10. Soenen V, Preudhomme C, Roumier C, Daudignon A, Lai JL, Fenaux P. 17p deletion in acute myeloid leukemia and myelodysplastic syndrome: analysis of breakpoints and deleted segments by fluorescence in situ. Blood. 1998;91:1008-1015.
11. Nakano Y, Naoe T, Kiyoi H, et al. Prognostic value of p53 gene mutations and the product expression in de novo acute myeloid leukemia. Eur J Haematol. 2000;65:23-31.
12. Wattel E, Preudhomme C, Hecquet B, et al. p53 mutations are associated with resistance to chemotherapy and short survival in hematologic malignancies. Blood. 1994;84:3148-3157.
13. Faderl S, Kantarjian HM, Estey E, et al. The prognostic significance of p16(INK4a)/ p14(ARF) locus deletion and MDM-2 protein expression in adult acute myelogenous leukemia. Cancer. 2000;89:1976-1982.
14. Seliger B, Papadileris S, Vogel D, et al. Analysis of the p53 and MDM-2 gene in acute myeloid leukemia. Eur J Haematol. 1996;57:230-240.
15. Bueso-Ramos CE, Yang Y, deLeon E, McCown P, Stass SA, Albitar M. The human MDM-2 oncogene is overexpressed in leukemias. Blood. 1993;82:2617-2623.
16. Moll UM, Petrenko O. The MDM2-p53 interaction. Mol Cancer Res. 2003;1:1001-1008.
17. Rich T, Allen RL, Wyllie AH. Defying death after DNA damage. Nature. 2000;407:777-783.
18. Zhou BB, Elledge SJ. The DNA damage response: putting checkpoints in perspective. Nature. 2000;408:433-439.
19. Vousden KH, Lu X. Live or let die: the cell's response to p53. Nat Rev Cancer. 2002;2:594-604.
20. Oda E, Ohki R, Murasawa H, et al. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science. 2000;288:1053-1058.
21. Nakano K, Vousden KH. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell. 2001;7:683-694.
22. Yu J, Zhang L, Hwang PM, Kinzler KW, Vogelstein B. PUMA induces the rapid apoptosis of colorectal cancer cells. Mol Cell. 2001;7:673-682.
23. Miyashita T, Reed JC. Tumor suppressor p53 is a direct transcriptional activator of the human BAX gene. Cell. 1995;80:293-299.
24. Chipuk JE, Kuwana T, Bouchier-Hayes L, et al. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science. 2004;303:1010-1014.
25. Leu JI, Dumont P, Hafey M, Murphy ME, George DL. Mitochondrial p53 activates Bak and causes disruption of a Bak-Mcl1 complex. Nat Cell Biol. 2004;6:443-450.
26. Mihara M, Erster S, Zaika A, et al. p53 has a direct apoptogenic role at the mitochondria. Mol Cell. 2003;11:577-590.
27. Vassilev LT, Vu BT, Graves B, et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science. 2004;303:844-848.
28. Matsuo Y, MacLeod RA, Uphoff CC, et al. Two acute monocytic leukemia (AML-M5a) cell lines (MOLM-13 and MOLM-14) with interclonal phenotypic heterogeneity showing MLL-AF9 fusion resulting from an occult chromosome insertion, ins(11;9)(q23;p22p23). Leukemia. 1997;11:1469-1477.
29. Wolf D, Rotter V. Major deletions in the gene encoding the p53 tumor antigen cause lack of p53 expression in HL-60 cells. Proc Natl Acad Sci U S A. 1985;82:790-794.
30. Fleckenstein DS, Uphoff CC, Drexler HG, Quentmeier H. Detection of p53 gene mutations by single strand conformational polymorphism (SSCP) in human acute myeloid leukemia-derived cell lines. Leuk Res. 2002;26:207-214.
31. Konopleva M, Tsao T, Ruvolo P, et al. Novel triterpenoid CDDO-Me is a potent inducer of apoptosis and differentiation in acute myelogenous leukemia. Blood. 2002;99:326-335.
32. Kato H, Kato S, Kumabe T, et al. Functional evaluation of p53 and PTEN gene mutations in gliomas. Clin Cancer Res. 2000;6:3937-3943.
33. 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.
34. Slovak ML, Kopecky KJ, Cassileth PA, et al. Karyotypic analysis predicts outcome of preremission and postremission therapy in adult acute myeloid leukemia: a Southwest Oncology Group/Eastern Cooperative Oncology Group Study. Blood. 2000;96:4075-4083.
35. Friesen C, Herr I, Krammer PH, Debatin KM. Involvement of the CD95 (APO-1/FAS) receptor/ligand system in drug-induced apoptosis in leukemia cells. Nat Med. 1996;2:574-577.
36. Kim IK, Lee JH, Sohn HW, Kim HS, Kim SH. Prostaglandin A2 and delta 12-prostaglandin J2 induce apoptosis in L1210 cells. FEBS Lett. 1993;321:209-214.
37. Bramwell VH, Morris D, Ernst DS, et al. Safety and efficacy of the multidrug-resistance inhibitor biricodar (VX-710) with concurrent doxorubicin in patients with anthracycline-resistant advanced soft tissue sarcoma. Clin Cancer Res. 2002;8:383-393.
38. Ling YH, el-Naggar AK, Priebe W, Perez-Soler R. Cell cycle-dependent cytotoxicity, G2/M phase arrest, and disruption of p34cdc2/cyclin B1 activity induced by doxorubicin in synchronized P388 cells. Mol Pharmacol. 1996;49:832-841.
39. Gachard N, Turlure P, Trimoreau F, et al. Quantification of MDM2 gene expression level by RQPCR is predictive of the first complete remission in adult acute myeloid leukemia [abstract]. Blood. 2004;104:303a. Abstract no. 1068.
40. Momand J, Jung D, Wilczynski S, Niland J. The MDM2 gene amplification database. Nucleic Acids Res. 1998;26:3453-3459.
41. Vassilev LT. Small-molecule antagonists of p53-MDM2 binding: research tools and potential therapeutics. Cell Cycle. 2004;3:419-421.
42. Zhang Z, Li M, Wang H, Agrawal S, Zhang R. Antisense therapy targeting MDM2 oncogene in prostate cancer: effects on proliferation, apoptosis, multiple gene expression, and chemotherapy. Proc Natl Acad Sci U S A. 2003;100:11636-11641.
43. Daujat S, Neel H, Piette J. MDM2: life without p53. Trends Genet. 2001;17:459-464.
44. Fischer PM, Lane DP. Small-molecule inhibitors of the p53 suppressor HDM2: have protein-protein interactions come of age as drug targets? Trends Pharmacol Sci. 2004;25:343-346.
45. Guzman ML, Swiderski CF, Howard DS, et al. Preferential induction of apoptosis for primary human leukemic stem cells. Proc Natl Acad Sci U S A. 2002;99:16220-16225.
46. Mendrysa SM, McElwee MK, Michalowski J, O'Leary KA, Young KM, Perry ME. mdm2 is critical for inhibition of p53 during lymphopoiesis and the response to ionizing irradiation. Mol Cell Biol. 2003;23:462-472.
47. Smart P, Lane EB, Lane DP, Midgley C, Vojtesek B, Lain S. Effects on normal fibroblasts and neuroblastoma cells of the activation of the p53 response by the nuclear export inhibitor leptomycin B. Oncogene. 1999;18:7378-7386.
48. Evan GI, Vousden KH. Proliferation, cell cycle and apoptosis in cancer. Nature. 2001;411:342-348.
49. Kakudo Y, Shibata H, Otsuka K, Kato S, Ishioka C. Lack of correlation between p53-dependent transcriptional activity and the ability to induce apoptosis among 179 mutant p53s. Cancer Res. 2005;65:2108-2114.
50. Arima Y, Nitta M, Kuninaka S, et al. Transcriptional blockade induces p53-dependent apoptosis associated with translocation of p53 to mitochondria. J Biol Chem. 2005;280:19166-19176.
51. Kanno S, Higurashi A, Watanabe Y, Shouji A, Asou K, Ishikawa M. Susceptibility to cytosine arabinoside (Ara-C)-induced cytotoxicity in human leukemia cell lines. Toxicol Lett. 2004;152:149-158.
52. Saito S, Yamaguchi H, Higashimoto Y, et al. Phosphorylation site interdependence of human p53 post-translational modifications in response to stress. J Biol Chem. 2003;278:37536-37544.
53. Brown JM, Wilson G. Apoptosis genes and resistance to cancer therapy: what does the experimental and clinical data tell us? Cancer Biol Ther. 2003;2:477-490.
54. Decker RH, Levin J, Kramer LB, Dai Y, Grant S. Enforced expression of the tumor suppressor p53 renders human leukemia cells (U937) more sensitive to 1-[beta-D-arabinofuranosyl]cytosine (ara-C)-induced apoptosis. Biochem Pharmacol. 2003;65:1997-2008.
55. Dunkern TR, Wedemeyer I, Baumgartner M, Fritz G, Kaina B. Resistance of p53 knockout cells to doxorubicin is related to reduced formation of DNA strand breaks rather than impaired apoptotic signaling. DNA Repair. 2003;2:49-60.
56. Ling YH, el-Naggar AK, Priebe W, Perez-Soler R. Cell cycle-dependent cytotoxicity, G2/M phase arrest, and disruption of p34cdc2/cyclin B1 activity induced by doxorubicin in synchronized P388 cells. Mol Pharmacol. 1996;49:832-841.
57. Radosevic N, Delmer A, Tang R, Marie JP, Ajchenbaum-Cymbalista F. Cell cycle regulatory protein expression in fresh acute myeloid leukemia cells and after drug exposure. Leukemia. 2001;15:559-566.
58. Masquelier M, Zhou QF, Gruber A, Vitols S. Relationship between daunorubicin concentration and apoptosis induction in leukemic cells. Biochem Pharmacol. 2004;67:1047-1056.
59. Del Poeta G, Venditti A, Del Principe MI, et al. Amount of spontaneous apoptosis detected by Bax/Bcl-2 ratio predicts outcome in acute myeloid leukemia (AML). Blood. 2003;101:2125-2131.
60. Carvajal D, Tovar C, Yang H, Vu BT, Heimbrook DC, Vassilev LT. Activation of p53 by MDM2 antagonists can protect proliferating cells from mitotic inhibitors. Cancer Res. 2005;65:1918-1924.