P53 stabilization induces apoptosis in chronic myeloid leukemia blast crisis cells

Leukemia

Volumn 25, Issue 5, 2011, Pages 761-769

  Peterson, L F ^a,b   Mitrikeska, E ^a,b   Giannola, D ^a,b   Lui, Y ^a,b   Sun, H ^a,b   Bixby, D ^a,b   Malek, S N ^a,b   Donato, N J ^a,b   Wang, S ^a   Talpaz, M ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

BCR ABL; CML; MDM2 inhibitor; p53; Philadelphia chromosome; therapy

Indexed keywords

BCR ABL PROTEIN; CASPASE; FAS ANTIGEN; IMATINIB; MI 219; MYC PROTEIN; PROTEIN BAX; PROTEIN BID; PROTEIN INHIBITOR; PROTEIN MCL 1; PROTEIN MDM2; PROTEIN NOXA; PROTEIN P53; PUMA PROTEIN; UNCLASSIFIED DRUG;

ADULT; AGED; APOPTOSIS; ARTICLE; BLAST CELL CRISIS; CHROMOSOME; CHRONIC MYELOID LEUKEMIA; CLINICAL ARTICLE; DOWN REGULATION; DRUG TARGETING; ENZYME ACTIVITY; FEMALE; GENE MUTATION; GENETIC TRANSCRIPTION; HUMAN; MALE; ONCOGENE C MYC; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN STABILITY;

ADULT; AGED; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; BLAST CRISIS; BLOTTING, WESTERN; FEMALE; FLOW CYTOMETRY; GENES, ABL; HUMANS; INDOLES; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MALE; MIDDLE AGED; MUTATION; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; PROTO-ONCOGENE PROTEINS C-MDM2; SPIRO COMPOUNDS; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53;

EID: 79955830260     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2011.7     Document Type: Article

References (69)

1. Nowell PC. Discovery of the Philadelphia chromosome: a personal perspective. J Clin Invest 2007; 117: 2033-2035. (Pubitemid 47219542)
2. Rowley JD. Chromosome translocations: dangerous liaisons revisited. Nat Rev Cancer 2001; 1: 245-250. (Pubitemid 33741900)
3. Matulonis U, Salgia R, Okuda K, Druker B, Griffin JD. Interleukin-3 and p210 BCR/ABL activate both unique and overlapping pathways of signal transduction in a factor-dependent myeloid cell line. Exp Hematol 1993; 21: 1460-1466. (Pubitemid 24215368)
4. Skorski T, Bellacosa A, Nieborowska-Skorska M, Majewski M, Martinez R, Choi JK et al. Transformation of hematopoietic cells by BCR/ABL requires activation of a PI-3k/Akt-dependent pathway. EMBO J 1997; 16: 6151-6161. (Pubitemid 27458335)
5. Xie S, Lin H, Sun T, Arlinghaus RB. Jak2 is involved in c-Myc induction by Bcr-Abl. Oncogene 2002; 21: 7137-7146. (Pubitemid 35305600)
6. Carlesso N, Frank DA, Griffin JD. Tyrosyl phosphorylation and DNA binding activity of signal transducers and activators of transcription (STAT) proteins in hematopoietic cell lines transformed by Bcr/Abl. J Exp Med 1996; 183: 811-820. (Pubitemid 26113953)
7. Perrotti D, Neviani P. From mRNA metabolism to cancer therapy: chronic myelogenous leukemia shows the way. Clin Cancer Res 2007; 13: 1638-1642. (Pubitemid 46952928)
8. Azam M, Latek RR, Daley GQ. Mechanisms of autoinhibition and STI-571/imatinib resistance revealed by mutagenesis of BCR-ABL. Cell 2003; 112: 831-843. (Pubitemid 36378885)
9. Gambacorti-Passerini CB, Gunby RH, Piazza R, Galietta A, Rostagno R, Scapozza L. Molecular mechanisms of resistance to imatinib in Philadelphia-chromosome-positive leukaemias. Lancet Oncol 2003; 4: 75-85. (Pubitemid 36196725)
10. Toledo F, Wahl GM. Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat Rev Cancer 2006; 6: 909-923. (Pubitemid 44862676)
11. Di Bacco A, Keeshan K, McKenna SL, Cotter TG. Molecular abnormalities in chronic myeloid leukemia: deregulation of cell growth and apoptosis. Oncologist 2000; 5: 405-415.
12. Trotta R, Vignudelli T, Candini O, Intine RV, Pecorari L, Guerzoni C et al. BCR/ABL activates mdm2 mRNA translation via the La antigen. Cancer Cell 2003; 3: 145-160. (Pubitemid 37443387)
13. Vousden KH, Lane DP. p53 in health and disease. Nat Rev Mol Cell Biol 2007; 8: 275-283. (Pubitemid 46474662)
14. Shu K-X, Li B, Wu L-X. The p53 network: p53 and its downstream genes. Colloids Surfaces B Biointerfaces 2007; 55: 10-18. (Pubitemid 46216062)
15. Riley T, Sontag E, Chen P, Levine A. Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 2008; 9: 402-412. (Pubitemid 351574202)
16. Steele AJ, Prentice AG, Hoffbrand AV, Yogashangary BC, Hart SM, Nacheva EP et al. p53-mediated apoptosis of CLL cells: evidence for a transcription-independent mechanism. Blood 2008; 112: 3827-3834.
17. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P et al. p53 has a direct apoptogenic role at the mitochondria. Mol Cell 2003; 11: 577-590. (Pubitemid 36385115)
18. Leu JIJ, Dumont P, Hafey M, Murphy ME, George DL. Mitochon-drial p53 activates Bak and causes disruption of a Bak-Mcl1 complex. Nat Cell Biol 2004; 6: 443-450. (Pubitemid 38607505)
19. Vassilev LT, Vu BT, Graves B, Carvajal D, Podlaski F, Filipovic Z et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 2004; 303: 844-848. (Pubitemid 38174664)
20. Shangary S, Qin D, McEachern D, Liu M, Miller RS, Qiu S et al. Temporal activation of p53 by a specific MDM2 inhibitor is selectively toxic to tumors and leads to complete tumor growth inhibition. Proc Natl Acad Sci USA 2008; 105: 3933-3938. (Pubitemid 351723502)
21. Ding K, Lu Y, Nikolovska-Coleska Z, Wang G, Qiu S, Shangary S et al. Structure-based design of spiro-oxindoles as potent, specific small-molecule inhibitors of the MDM2&. J Med Chem 2006; 49: 3432-3435. (Pubitemid 43902447)
22. Shangary S, Wang S. Small-molecule inhibitors of the MDM2-p53 protein-protein interaction to reactivate p53 function: a novel approach for cancer therapy. Annu Rev Pharmacol Toxicol 2009; 49: 223.
23. Saddler C, Ouillette P, Kujawski L, Shangary S, Talpaz M, Kaminski M et al. Comprehensive biomarker and genomic analysis identifies p53 status as the major determinant of response to MDM2 inhibitors in chronic lymphocytic leukemia. Blood 2008; 111: 1584-1593. (Pubitemid 351213449)
24. Brummelkamp TR, Bernards R, Agami R. A system for stable expression of short interfering RNAs in mammalian cells. Science 2002; 296: 550-553. (Pubitemid 34408678)
25. Alves NL, Derks IAM, Berk E, Spijker R, van Lier RAW, Eldering E. The Noxa/Mcl-1 axis regulates susceptibility to apoptosis under glucose limitation in dividing T cells. Immunity 2006; 24: 703-716. (Pubitemid 43867360)
26. Peterson LF, Wang Y, Lo MC, Yan M, Kanbe E, Zhang DE. The multifunctional cellular adhesion molecule CD44 is regulated by the 8;21 chromosomal translocation. Leukemia 2007; 21: 2010-2019. (Pubitemid 47303957)
27. Keeshan K, Cotter TG, McKenna SL. High Bcr-Abl expression prevents the translocation of Bax and Bad to the mitochondrion. Leukemia 2002; 16: 1725-1734.
28. Vassilev LT. MDM2 inhibitors for cancer therapy. Trends Mol Med 2007; 13: 23-31. (Pubitemid 46027725)
29. Soldani C, Scovassi AI. Poly(ADP-ribose) polymerase-1 cleavage during apoptosis: an update. Apoptosis 2002; 7: 321-328. (Pubitemid 34832256)
30. Oda T, Heaney C, Hagopian JR, Okuda K, Griffin JD, Druker BJ. Crkl is the major tyrosine-phosphorylated protein in neutrophils from patients with chronic myelogenous leukemia. J Biol Chem 1994; 269: 22925-22928. (Pubitemid 24283264)
31. Lau LM, Nugent JK, Zhao X, Irwin MS. HDM2 antagonist Nutlin-3 disrupts p73-HDM2 binding and enhances p73 function. Onco-gene 2008; 27: 997-1003. (Pubitemid 351225385)
32. Bartholomeusz GA, Talpaz M, Kapuria V, Kong LY, Wang S, Estrov Z et al. Activation of a novel Bcr/Abl destruction pathway by WP1130 induces apoptosis of chronic myelogenous leukemia cells. Blood 2007; 109: 3470-3478. (Pubitemid 46572537)
33. Aichberger KJ, Mayerhofer M, Krauth MT, Skvara H, Florian S, Sonneck K et al. 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 oligonu-cleotides. Blood 2005; 105: 3303-3311.
34. Lovell JF, Billen LP, Bindner S, Shamas-Din A, Fradin C, Leber B et al. Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by bax. Cell 2008; 135: 1074-1084.
35. Xia M, Knezevic D, Tovar C, Huang B, Heimbrook DC, Vassilev LT. Elevated MDM2 boosts the apoptotic activity of p53-MDM2 binding inhibitors by facilitating MDMX degradation. Cell Cycle 2008; 7: 1604-1612. (Pubitemid 351881328)
36. Donato NJ, Wu JY, Stapley J, Gallick G, Lin H, Arlinghaus R et al. BCR-ABL independence and LYN kinase overexpression in chronic myelogenous leukemia cells selected for resistance to STI571. Blood 2003; 101: 690-698. (Pubitemid 36077594)
37. Muller M, Wilder S, Bannasch D, Israeli D, Lehlbach K, Li-Weber M et al. p53 activates the CD95 (APO-1/Fas) gene in response to DNA damage by anticancer drugs. J Exp Med 1998; 188: 2033-2045. (Pubitemid 28562520)
38. Ow Y-LP, Green DR, Hao Z, Mak TW. Cytochrome c: functions beyond respiration. Nat Rev Mol Cell Biol 2008; 9: 532-542. (Pubitemid 351881842)
39. Vaseva AV, Moll UM. The mitochondrial p53 pathway. Biochim Biophys Acta (BBA)FBioenergetics 2009; 1787: 414-420.
40. Ploner C, Kofler R, Villunger A. Noxa: at the tip of the balance between life and death. Oncogene 2009; 27 (S1): S84-S92.
41. Selleri C, Sato T, Del Vecchio L, Luciano L, Barrett AJ, Rotoli B et al. Involvement of Fas-mediated apoptosis in the inhibitory effects of interferon-alpha in chronic myelogenous leukemia. Blood 1997; 89: 957-964. (Pubitemid 27121289)
42. Sancho-Martinez I, Martin-Villalba A. Tyrosine phosphorylation and CD95: a FAScinating switch. Cell Cycle 2009; 8: 838-842.
43. Ametller E, Garcia-Recio S, Costamagna D, Mayordomo C, Fernandez-Nogueira P, Carbo N et al. Tumor promoting effects of CD95 signaling in chemoresistant cells. Mol Cancer 2010; 9: 161.
44. Druker BJ. Translation of the Philadelphia chromosome into therapy for CML. Blood 2008; 112: 4808-4817.
45. 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: 2242-2249. (Pubitemid 47523141)
46. Shah NP, Sawyers CL. Mechanisms of resistance to STI571 in Philadelphia chromosome-associated leukemias. Oncogene 2003; 22: 7389-7395. (Pubitemid 37487164)
47. Kujawski L, Talpaz M. Strategies for overcoming imatinib resistance in chronic myeloid leukemia. Leuk Lymphoma 2007; 48: 2310-2322. (Pubitemid 350253462)
48. Graham SM, Jorgensen HG, Allan E, Pearson C, Alcorn MJ, Richmond L et al. Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. Blood 2002; 99: 319-325.
49. Jorgensen HG, Allan EK, Jordanides NE, Mountford JC, Holyoake TL. Nilotinib exerts equipotent antiproliferative effects to imatinib and does not induce apoptosis in CD34+ CML cells. Blood2007;109: 4016-4019.
50. Copland M, Hamilton A, Elrick LJ, BairdJW, Allan EK, Jordanides N 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: 4532-4539. (Pubitemid 43801382)
51. Seliger B, Papadileris S, Vogel D, Hess G, Brendel C, Storkel S et al. Analysis of the p53 and MDM-2 gene in acute myeloid leukemia. EurJ Haematol 1996; 57: 230-240. (Pubitemid 26346036)
52. ChangJS, Santhanam R, Trotta R, Neviani P, Eiring AM, Briercheck E et al. High levels of the BCR/ABL oncoprotein are required for the MAPK-hnRNP-E2 dependent suppression of C/EBP alpha-driven myeloid differentiation. Blood 2007; 110: 994-1003. (Pubitemid 47267439)
53. Notari M, Neviani P, Santhanam R, Blaser BW, ChangJS, Galietta A et al. A MAPK/HNRPK pathway controls BCR/ABL oncogenic potential by regulating MYC mRNA translation. Blood 2006; 107: 2507-2516. (Pubitemid 43345575)
54. Eiring AM, Neviani P, Santhanam R, Oaks JJ, ChangJS, Notari M et al. Identification of novel posttranscriptional targets of the BCR/ ABL oncoprotein by ribonomics: requirement of E2F3 for BCR/ABL leukemogenesis. Blood 2008; 111: 816-828.
55. Komarova EA, Kondratov RV, Wang K, Christov K, Golovkina TV, Goldblum JR et al. Dual effect of p53 on radiation sensitivity in vivo: p53 promotes hematopoietic injury, but protects from gastrointestinal syndrome in mice. Oncogene 2004; 23: 3265-3271. (Pubitemid 38669816)
56. Liu Y, Elf SE, Miyata Y, Sashida G, Huang G, Di Giandomenico S etal. p53 regulates hematopoietic stem cell quiescence. Cell Stem Cell 2009; 4: 37-48.
57. Akala OO, Park I-K, Qian D, Pihalja M, Becker MW, Clarke MF. Long-term haematopoietic reconstitution by Trp53-/-p16Ink4a-/ -p19Arf-/- multipotent progenitors. Nature2008; 453: 228-232. (Pubitemid 351667977)
58. Coll-Mulet L, Iglesias-Serret D, Santidrian AF, Cosialls AM, de Frias M, Castano E etal. MDM2 antagonists activate p53 and synergize with genotoxic drugs in B-cell chronic lymphocytic leukemia cells. Blood 2006; 107: 4109-4114. (Pubitemid 43726820)
59. Sawyers CL, Hochhaus A, Feldman E, Goldman JM, Miller CB, Ottmann OG etal. Imatinib induces hematologic and cytogenetic responses in patients with chronic myelogenous leukemia in myeloid blast crisis: results of a phase II study. Blood 2002; 99: 3530-3539. (Pubitemid 34534519)
60. Talpaz M, Silver RT, Druker BJ, Goldman JM, Gambacorti-Passerini C, Guilhot F etal. Imatinib induces durable hematologic and cytogenetic responses in patients with accelerated phase chronic myeloid leukemia: results of a phase 2 study. Blood2002; 99: 1928-1937. (Pubitemid 34525471)
61. Jamieson CH, Ailles LE, Dylla SJ, Muijtjens M, Jones C, Zehnder JL etal. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N EnglJ Med2004; 351: 657-667. (Pubitemid 39063268)
62. Abrahamsson AE, Geron I, Gotlib J, Dao K-HT, Barroga CF, Newton IG et al. Glycogen synthase kinase 3-3 missplicing contributes to leukemia stem cell generation. Proc Natl Acad Sci USA 2009; 106: 3925-3929.
63. Zhao C, Blum J, Chen A, Kwon HY, Jung SH, Cook JM et al. Loss of beta-catenin impairs the renewal of normal and CML stem cells in vivo. Cancer Cell 2007; 12: 528-541. (Pubitemid 350199070)
64. Zhao C, Chen A, Jamieson CH, Fereshteh M, Abrahamsson A, Blum J et al. Hedgehog signalling is essential for maintenance of cancer stem cells in myeloid leukaemia. Nature 2009; 458: 776-779.
65. Stecca B, Ruizi Altaba A. A GLI1 -p53 inhibitory loop controls neural stem cell and tumour cell numbers. EMBO J 2009; 28: 663-676.
66. Prowald A, Cronauer MV, von Klot C, Eilers T, Rinnab L, Herrmann T et al. Modulation of beta-catenin-mediated TCF-signalling in prostate cancer cell lines by wild-type and mutant p53. Prostate 2007; 67: 1751-1760. (Pubitemid 350228727)
67. Rother K, Johne C, Spiesbach K, Haugwitz U, Tschop K, Wasner M et al. Identification of Tcf-4 as a transcriptional target of p53 signalling. Oncogene 2004; 23: 3376-3384. (Pubitemid 38669827)
68. Abe Y, Oda-Sato E, Tobiume K, Kawauchi K, Taya Y, Okamoto K et al. Hedgehog signaling overrides p53-mediated tumor suppression by activating Mdm2. Proc Natl Acad Sci USA 2008; 105: 4838-4843. (Pubitemid 351753833)
69. Long J, Parkin B, Ouillette P, Bixby D, Shedden K, Erba H etal. Multiple distinct molecular mechanisms influence sensitivity and resistance to MDM2 inhibitors in adult acute myelogenous leukemia. Blood 2010; 116: 71-80.