Treatment with a BH3 mimetic overcomes the resistance of latency III EBV (+) cells to p53-mediated apoptosis

Cell Death and Disease

Volumn 2, Issue 7, 2011, Pages

  Pujals, A ^a   Renouf, B ^a,b   Robert, A ^a   Chelouah, S ^a   Hollville, E ^a,c   Wiels, J ^a  

^a UMR 8126   (France)

^b HÔPITAL DE HAUTEPIERRE   (France)

^c TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

apoptosis; Bax; Bcl 2; Burkitt's lymphoma; EBV; p53

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; BH3 PROTEIN; NUTLIN 3; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; ABT-737; BIPHENYL DERIVATIVE; IMIDAZOLE DERIVATIVE; NITROPHENOL; PIPERAZINE DERIVATIVE; PROTEIN MDM2; SULFONAMIDE;

APOPTOSIS; ARTICLE; BURKITT LYMPHOMA; CONTROLLED STUDY; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; LYMPHOBLASTOID CELL LINE; LYMPHOMA CELL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; DRUG ANTAGONISM; DRUG EFFECT; ISOLATION AND PURIFICATION; METABOLISM; MITOCHONDRION; TUMOR CELL LINE;

HUMAN HERPESVIRUS 4; MURINAE;

APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BIPHENYL COMPOUNDS; CELL LINE, TUMOR; HERPESVIRUS 4, HUMAN; HUMANS; IMIDAZOLES; MITOCHONDRIA; NITROPHENOLS; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-BCL-2; PROTO-ONCOGENE PROTEINS C-MDM2; SULFONAMIDES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 80051527422     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2011.67     Document Type: Article

References (40)

1. Lane DP. Cancer. p53, guardian of the genome. Nature 1992; 358: 15-16.
2. Levine AJ. p53, the cellular gatekeeper for growth and division. Cell 1997; 88: 323-331. (Pubitemid 27131374)
3. Vousden KH, Lu X. Live or let die: The cell's response to p53. Nat Rev Cancer 2002; 2: 594-604. (Pubitemid 37328926)
4. Honda R, Tanaka H, Yasuda H. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett 1997; 420: 25-27. (Pubitemid 28037193)
5. Momand J, Zambetti GP, Olson DC, George D, Levine AJ. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 1992; 69: 1237-1245.
6. Capoulade C, Bressac-de Paillerets B, Lefrere I, Ronsin M, Feunteun J, Tursz T et al. Overexpression of MDM2, due to enhanced translation, results in inactivation of wild-type p53 in Burkitt's lymphoma cells. Oncogene 1998; 16: 1603-1610. (Pubitemid 28159908)
7. Oliner JD, Kinzler KW, Meltzer PS, George DL, Vogelstein B. Amplification of a gene encoding a p53-associated protein in human sarcomas. Nature 1992; 358: 80-83.
8. Dickens MP, Fitzgerald R, Fischer PM. Small-molecule inhibitors of MDM2 as new anticancer therapeutics. Semin Cancer Biol 2010; 20: 10-18.
9. Yang Y, Ludwig RL, Jensen JP, Pierre SA, Medaglia MV, Davydov IV et al. Small molecule inhibitors of HDM2 ubiquitin ligase activity stabilize and activate p53 in cells. Cancer Cell 2005; 7: 547-559. (Pubitemid 40799248)
10. 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)
11. Stuhmer T, Chatterjee M, Hildebrandt M, Herrmann P, Gollasch H, Gerecke C et al. Nongenotoxic activation of the p53 pathway as a therapeutic strategy for multiple myeloma. Blood 2005; 106: 3609-3617. (Pubitemid 41609200)
12. Sarek G, Kurki S, Enback J, Iotzova G, Haas J, Laakkonen P et al. Reactivation of the p53 pathway as a treatment modality for KSHV-induced lymphomas. J Clin Invest 2007; 117: 1019-1028. (Pubitemid 46556758)
13. Van Maerken T, Ferdinande L, Taildeman J, Lambertz I, Yigit N, Vercruysse L et al. Antitumor activity of the selective MDM2 antagonist nutlin-3 against chemoresistant neuroblastoma with wild-type p53. J Natl Cancer Inst 2009; 101: 1562-1574.
14. Vassilev LT. MDM2 inhibitors for cancer therapy. Trends Mol Med 2007; 13: 23-31. (Pubitemid 46027725)
15. Vazquez A, Bond EE, Levine AJ, Bond GL. The genetics of the p53 pathway, apoptosis and cancer therapy. Nat Rev Drug Discov 2008; 7: 979-987.
16. Spierings D, McStay G, Saleh M, Bender C, Chipuk J, Maurer U et al. Connected to death: The (unexpurgated) mitochondrial pathway of apoptosis. Science 2005; 310: 66-67. (Pubitemid 41434533)
17. Youle RJ, Strasser A. The BCL-2 protein family: Opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008; 9: 47-59.
18. Chipuk JE, Green DR. How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol 2008; 18: 157-164.
19. Schuler M, Green DR. Transcription, apoptosis and p53: Catch-22. Trends Genet 2005; 21: 182-187. (Pubitemid 40269857)
20. Lindstrom MS, Wiman KG. Role of genetic and epigenetic changes in Burkitt lymphoma. Semin Cancer Biol 2002; 12: 381-387.
21. Renouf B, Hollville E, Pujals A, Tetaud C, Garibal J, Wiels J. Activation of p53 by MDM2 antagonists has differential apoptotic effects on Epstein-Barr virus (EBV)-positive and EBV-negative Burkitt's lymphoma cells. Leukemia 2009; 23: 1557-1563.
22. Thompson MP, Kurzrock R. Epstein-Barr virus and cancer. Clin Cancer Res 2004; 10: 803-821. (Pubitemid 38198878)
23. Rowe M, Rowe DT, Gregory CD, Young LS, Farrell PJ, Rupani H et al. Differences in B-cell growth phenotype reflect novel patterns of Epstein-Barr virus latent gene expression in Burkitt's lymphoma cells. EMBO J 1987; 6: 2743-2751.
24. OoNions J, Allday MJ. Epstein-Barr virus can inhibit genotoxin-induced G1 arrest downstream of p53 by preventing the inactivation of CDK2. Oncogene 2003; 22: 7181-7191. (Pubitemid 37378550)
25. Okan I, Wang Y, Chen F, Hu LF, Imreh S, Klein G et al. The EBV-encoded LMP1 protein inhibits p53-triggered apoptosis but not growth arrest. Oncogene 1995; 11: 1027-1031.
26. Hsu YT, Youle RJ. Bax in murine thymus is a soluble monomeric protein that displays differential detergent-induced conformations. J Biol Chem 1998; 273: 10777-10783. (Pubitemid 28227695)
27. Portis T, Longnecker R. Epstein-Barr virus (EBV) LMP2A mediates B-lymphocyte survival through constitutive activation of the Ras/PI3K/Akt pathway. Oncogene 2004; 23: 8619-8628. (Pubitemid 39576469)
28. Rowe M, Peng-Pilon M, Huen DS, Hardy R, Croom-Carter D, Lundgren E et al. Upregulation of bcl-2 by the Epstein-Barr virus latent membrane protein LMP1: A B-cellspecific response that is delayed relative to NF-kappa B activation and to induction of cell surface markers. J Virol 1994; 68: 5602-5612. (Pubitemid 24258573)
29. Wang S, Rowe M, Lundgren E. Expression of the Epstein Barr virus transforming protein LMP1 causes a rapid and transient stimulation of the Bcl-2 homologue Mcl-1 levels in B-cell lines. Cancer Res 1996; 56: 4610-4613. (Pubitemid 26338058)
30. Grimm T, Schneider S, Naschberger E, Huber J, Guenzi E, Kieser A et al. EBV latent membrane protein-1 protects B cells from apoptosis by inhibition of BAX. Blood 2005; 105: 3263-3269.
31. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, Belli BA et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 2005; 435: 677-681. (Pubitemid 40825512)
32. Farnebo M, Bykov VJ, Wiman KG. The p53 tumor suppressor: A master regulator of diverse cellular processes and therapeutic target in cancer. Biochem Biophys Res Commun 2010; 396: 85-89.
33. Nechushtan A, Smith CL, Hsu YT, Youle RJ. Conformation of the Bax C-terminus regulates subcellular location and cell death. EMBO J 1999; 18: 2330-2341. (Pubitemid 29213267)
34. Murphy KM, Ranganathan V, Farnsworth ML, Kavallaris M, Lock RB. Bcl-2 inhibits Bax translocation from cytosol to mitochondria during drug-induced apoptosis of human tumor cells. Cell Death Differ 2000; 7: 102-111. (Pubitemid 30153768)
35. Murphy KM, Streips UN, Lock RB. Bcl-2 inhibits a Fas-induced conformational change in the Bax N terminus and Bax mitochondrial translocation. J Biol Chem 2000; 275: 17225-17228. (Pubitemid 30430751)
36. Forte E, Luftig MA. MDM2-dependent inhibition of p53 is required for Epstein-Barr virus B-cell growth transformation and infected-cell survival. J Virol 2009; 83: 2491-2499.
37. Feuillard J, Schuhmacher M, Kohanna S, Asso-Bonnet M, Ledeur F, Joubert-Caron R et al. Inducible loss of NF-kappaB activity is associated with apoptosis and Bcl-2 down-regulation in Epstein-Barr virus-transformed B lymphocytes. Blood 2000; 95: 2068-2075. (Pubitemid 30151647)
38. Kojima K, Konopleva M, Samudio IJ, Schober WD, Bornmann WG, Andreeff M. Concomitant inhibition of MDM2 and Bcl-2 protein function synergistically induce mitochondrial apoptosis in AML. Cell Cycle 2006; 5: 2778-2786. (Pubitemid 44901740)
39. Wade M, Rodewald LW, Espinosa JM, Wahl GM. BH3 activation blocks Hdmx suppression of apoptosis and cooperates with Nutlin to induce cell death. Cell Cycle 2008; 7: 1973-1982. (Pubitemid 352030342)
40. Murray PG, Swinnen LJ, Constandinou CM, Pyle JM, Carr TJ, Hardwick JM et al. BCL-2 but not its Epstein-Barr virus-encoded homologue, BHRF1, is commonly expressed in posttransplantation lymphoproliferative disorders. Blood 1996; 87: 706-711. (Pubitemid 26030326)