MYCN sensitizes neuroblastoma to the MDM2-p53 antagonists Nutlin-3 and MI-63

Oncogene

Volumn 31, Issue 6, 2012, Pages 752-763

  Gamble, L D ^a   Kees, U R ^b   Tweddle, D A ^a   Lunec, J ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

apoptosis; growth inhibition; MDM2 p53 antagonists; MYCN; neuroblastoma

Indexed keywords

ANTINEOPLASTIC AGENT; CASPASE 3; CASPASE 7; CYCLIN DEPENDENT KINASE INHIBITOR 2A; MI 63; MYC PROTEIN; NUTLIN 3; PROTEIN INHIBITOR; PROTEIN MDM2; PROTEIN P53; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE REGULATION; ENZYME ACTIVITY; GENE AMPLIFICATION; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSCRIPTION; GROWTH INHIBITION; NEUROBLASTOMA; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

APOPTOSIS; BLOTTING, WESTERN; CASPASE 3; CASPASE 7; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; FLOW CYTOMETRY; HUMANS; IMIDAZOLES; INDOLES; MODELS, BIOLOGICAL; MUTATION; NUCLEAR PROTEINS; ONCOGENE PROTEINS; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-MDM2; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SPIRO COMPOUNDS; TETRACYCLINE; TUMOR SUPPRESSOR PROTEIN P14ARF; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84856961064     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.270     Document Type: Article

References (44)

1. Alt JR, Greiner TC, Cleveland JL, Eischen CM. (2003). Mdm2 haploinsufficiency profoundly inhibits Myc-induced lymphomagenesis. Embo J 22: 1442-1450. (Pubitemid 36362707)
2. Amente S, Gargano B, Diolaiti D, Della Valle G, Lania L, Majello B. (2007). p14ARF interacts with N-Myc and inhibits its transcriptional activity. FEBS Lett 581: 821-825. (Pubitemid 46282710)
3. Barbieri E, Mehta P, Chen Z, Zhang L, Slack A, Berg S et al. (2006). MDM2 inhibition sensitizes neuroblastoma to chemotherapyinduced apoptotic cell death. Mol Cancer Ther 5: 2358-2365. (Pubitemid 44530473)
4. Bell E, Premkumar R, Carr J, Lu X, Lovat PE, Kees UR et al. (2006). The role of MYCN in the failure of MYCN amplified neuroblastoma cell lines to G1 arrest after DNA damage. Cell Cycle 5: 2639-2647. (Pubitemid 44785808)
5. Canner JA, Sobo M, Ball S, Hutzen B, DeAngelis S, Willis W et al. (2009). MI-63: a novel small-molecule inhibitor targets MDM2 and induces apoptosis in embryonal and alveolar rhabdomyosarcoma cells with wild-type p53. Br J Cancer 101: 774-781.
6. Carr-Wilkinson J, O'Toole K, Wood KM, Challen CC, Baker AG, Board JR et al. (2010). High frequency of p53/MDM2/p14ARF pathway abnormalities in relapsed neuroblastoma. Clin Cancer Res 16: 1108-1118.
7. Carr J, Bell E, Pearson AD, Kees UR, Beris H, Lunec J et al. (2006). Increased frequency of aberrations in the p53/MDM2/p14(ARF) pathway in neuroblastoma cell lines established at relapse. Cancer Res 66: 2138-2145.
8. Chen L, Iraci N, Gherardi S, Gamble LD, Wood KM, Perini G et al. (2010). p53 is a direct transcriptional target of MYCN in neuroblastoma. Cancer Res 70: 1377-1388.
9. Chen Z, Lin Y, Barbieri E, Burlingame S, Hicks J, Ludwig A et al. (2009). Mdm2 deficiency suppresses MYCN-Driven neuroblastoma tumorigenesis in vivo. Neoplasia 11: 753-762.
10. Chipuk JE, Green DR. (2006). Dissecting p53-dependent apoptosis. Cell Death Differ 13: 994-1002.
11. Cohn SL, Pearson AD, London WB, Monclair T, Ambros PF, Brodeur GM et al. (2009). The International Neuroblastoma Risk Group (INRG) classification system: an INRG Task Force report. J Clin Oncol 27: 289-297.
12. Cohn SL, Tweddle DA. (2004). MYCN amplification remains prognostically strong 20 years after its 'clinical debut'. Eur J Cancer 40: 2639-2642. (Pubitemid 39574716)
13. Corvi R, Savelyeva L, Breit S, Wenzel A, Handgretinger R, Barak J et al. (1995). Non-syntenic amplification of MDM2 and MYCN in human neuroblastoma. Oncogene 10: 1081-1086.
14. Demidenko ZN, Korotchkina LG, Gudkov AV, Blagosklonny MV. (2010). Paradoxical suppression of cellular senescence by p53. Proc Natl Acad Sci USA 107: 9660-9664.
15. Efeyan A, Ortega-Molina A, Velasco-Miguel S, Herranz D, Vassilev LT, Serrano M. (2007). Induction of p53-dependent senescence by the MDM2 antagonist nutlin-3a in mouse cells of fibroblast origin. Cancer Res 67: 7350-7357. (Pubitemid 47206565)
16. Fulda S, Lutz W, Schwab M, Debatin KM. (2000). MycN sensitizes neuroblastoma cells for drug-triggered apoptosis. Med Pediatr Oncol 35: 582-584.
17. Goldman SC, Chen CY, Lansing TJ, Gilmer TM, Kastan MB. (1996). The p53 signal transduction pathway is intact in human neuroblastoma despite cytoplasmic localization. Am J Pathol 148: 1381-1385. (Pubitemid 26135882)
18. Hogarty MD. (2003). The requirement for evasion of programmed cell death in neuroblastomas with MYCN amplification. Cancer Lett 197: 173-179. (Pubitemid 36860007)
19. Hosoi G, Hara J, Okamura T, Osugi Y, Ishihara S, FukuzawaM et al. (1994). Low frequency of the p53 gene mutations in neuroblastoma. Cancer 73: 3087-3093. (Pubitemid 24170786)
20. Kang JH, Rychahou PG, Ishola TA, Qiao J, Evers BM, Chung DH. (2006). MYCN silencing induces differentiation and apoptosis in human neuroblastoma cells. Biochem Biophys Res Commun 351: 192-197. (Pubitemid 44635425)
21. Kojima K, Konopleva M, Samudio IJ, Shikami M, Cabreira-Hansen M, McQueen T et al. (2005). MDM2 antagonists induce p53-dependent apoptosis in AML: implications for leukemia therapy. Blood 106: 3150-3159. (Pubitemid 41565913)
22. Korotchkina LG, Leontieva OV, Bukreeva EI, Demidenko ZN, Gudkov AV, Blagosklonny MV. (2010). The choice between p53-induced senescence and quiescence is determined in part by the mTOR pathway. Aging (Albany NY) 2: 344-352.
23. Lutz W, Stohr M, Schurmann J, Wenzel A, Lohr A, Schwab M. (1996). Conditional expression of N-myc in human neuroblastoma cells increases expression of alpha-prothymosin and ornithine decarboxylase and accelerates progression into S-phase early after mitogenic stimulation of quiescent cells. Oncogene 13: 803-812. (Pubitemid 26312908)
24. Maris JM, Hogarty MD, Bagatell R, Cohn SL. (2007). Neuroblastoma. Lancet 369: 2106-2120. (Pubitemid 46935947)
25. Maris JM, Matthay KK. (1999). Molecular biology of neuroblastoma. J Clin Oncol 17: 2264-2279. (Pubitemid 29318861)
26. Matthay KK, Villablanca JG, Seeger RC, Stram DO, Harris RE, Ramsay NK et al. (1999). Treatment of high-risk neuroblastoma with intensive chemotherapy, radiotherapy, autologous bone marrow transplantation, and 13-cis-retinoic acid. Children's Cancer Group. N Engl J Med 341: 1165-1173. (Pubitemid 29480654)
27. Michalak E, Villunger A, Erlacher M, Strasser A. (2005). Death squads enlisted by the tumour suppressor p53.Biochem Biophys Res Commun 331: 786-798. (Pubitemid 40615509)
28. Muller CR, Paulsen EB, Noordhuis P, Pedeutour F, Saeter G, Myklebost O. (2007). Potential for treatment of liposarcomas with the MDM2 antagonist Nutlin-3A. Int J Cancer 121: 199-205. (Pubitemid 46753868)
29. Petroni M, Veschi V, Prodosmo A, Rinaldo C, Massimi I, Carbonari M et al. (2011). MYCN sensitizes human neuroblastoma to apoptosis by HIPK2 activation through a DNA damage response. Mol Cancer Res 9: 67-77.
30. Skehan P, Storeng R, Scudiero D, Monks A, McMahon J, Vistica D et al. (1990). New colorimetric cytotoxicity assay for anticancerdrug screening. J Natl Cancer Inst 82: 1107-1112. (Pubitemid 20213250)
31. Slack A, Chen Z, Tonelli R, Pule M, Hunt L, Pession A et al. (2005). The p53 regulatory gene MDM2 is a direct transcriptional target of MYCN in neuroblastoma. Proc Natl Acad Sci USA 102: 731-736. (Pubitemid 40282734)
32. Slack A, Shohet JM. (2005). MDM2 as a critical effector of the MYCN oncogene in tumorigenesis. Cell Cycle 4: 857-860. (Pubitemid 41359744)
33. Tweddle DA, Malcolm AJ, Cole M, Pearson AD, Lunec J. (2001). p53 cellular localization and function in neuroblastoma: evidence for defective G(1) arrest despite WAF1 induction in MYCN-amplified cells. Am J Pathol 158: 2067-2077. (Pubitemid 32545192)
34. Tweddle DA, Pearson AD, Haber M, Norris MD, Xue C, Flemming C et al. (2003). The p53 pathway and its inactivation in neuroblastoma. Cancer Lett 197: 93-98. (Pubitemid 36859996)
35. Van Maerken T, Rihani A, Dreidax D, De Clercq S, Yigit N, Marine JC et al. (2011). Functional analysis of the p53 pathway in neuroblastoma cells using the small-molecule MDM2 antagonist nutlin-3. Mol Cancer Ther 10: 983-993.
36. Van Maerken T, Speleman F, Vermeulen J, Lambertz I, De Clercq S, De Smet E et al. (2006). Small-molecule MDM2 antagonists as a new therapy concept for neuroblastoma. Cancer Res 66: 9646-9655. (Pubitemid 44623664)
37. van Noesel MM, Pieters R, Voute PA, Versteeg R. (2003). The N-myc paradox: N-myc overexpression in neuroblastomas is associated with sensitivity as well as resistance to apoptosis. Cancer Lett 197: 165-172. (Pubitemid 36860006)
38. van Noesel MM, Versteeg R. (2004). Pediatric neuroblastomas: genetic and epigenetic 'danse macabre'. Gene 325: 1-15. (Pubitemid 38030371)
39. Vassilev LT, Vu BT, Graves B, Carvajal D, Podlaski F, Filipovic Z et al. (2004). In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303: 844-848. (Pubitemid 38174664)
40. Vogan K, Bernstein M, Leclerc JM, Brisson L, Brossard J, Brodeur GM et al. (1993). Absence of p53 gene mutations in primary neuroblastomas. Cancer Res 53: 5269-5273. (Pubitemid 23333398)
41. Wang P, Greiner TC, Lushnikova T, Eischen CM. (2006). Decreased Mdm2 expression inhibits tumor development induced by loss of ARF. Oncogene 25: 3708-3718. (Pubitemid 43980492)
42. Weiss WA, Aldape K, Mohapatra G, Feuerstein BG, Bishop JM. (1997). Targeted expression of MYCN causes neuroblastoma in transgenic mice. Embo J 16: 2985-2995. (Pubitemid 27234938)
43. Wenzel A, Cziepluch C, Hamann U, Schurmann J, Schwab M. (1991). The N-Myc oncoprotein is associated in vivo with the phosphoprotein Max(p20/22) in human neuroblastoma cells. Embo J 10: 3703-3712. (Pubitemid 21905397)
44. Zindy F, Eischen CM, Randle DH, Kamijo T, Cleveland JL, Sherr CJ et al. (1998). Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev 12: 2424-2433. (Pubitemid 28371361)