MYCN sensitizes human neuroblastoma to apoptosis by HIPK2 activation through a DNA damage response

Molecular Cancer Research

Volumn 9, Issue 1, 2011, Pages 67-77

  Petroni, Marialaura ^a   Veschi, Veronica ^a   Prodosmo, Andrea ^b   Rinaldo, Cinzia ^b   Massimi, Isabella ^a   Carbonari, Maurizio ^a   Dominici, Carlo ^a,c,d   McDowell, Heather P ^a,e   Rinaldi, Christian ^a   Screpanti, Isabella ^a   Frati, Luigi ^a   Bartolazzi, Armando ^f   Gulino, Alberto ^a,g   Soddu, Silvia ^b   Giannini, Giuseppe ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^c BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^d UNIVERSITY OF LIVERPOOL   (United Kingdom)

^e ALDER HEY CHILDREN'S NHS FOUNDATION TRUST   (United Kingdom)

^f SAPIENZA UNIVERSITY OF ROME   (Italy)

^g IRCCS NEUROMED   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN INTERACTING PROTEIN KINASE 2; MYC PROTEIN; NUTLIN 3; PROTEIN MYCN; PROTEIN P53; SERINE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL POPULATION; DNA DAMAGE; ENZYME ACTIVATION; HUMAN; HUMAN CELL; NEUROBLASTOMA; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE;

ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; BLEOMYCIN; BLOTTING, WESTERN; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; DNA DAMAGE; DNA-BINDING PROTEINS; HUMANS; MUTATION; NEUROBLASTOMA; NUCLEAR PROTEINS; ONCOGENE PROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE; SERINE; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 78751539761     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-10-0227     Document Type: Article

References (55)

1. Maris JM, Matthay KK. Molecular biology of neuroblastoma. J Clin Oncol 1999;17:2264-79.
2. Brodeur GM. Neuroblastoma: biological insights into a clinical enigma. Nat Rev Cancer 2003;3:203-16.
3. Cohn SL, Pearson AD, London WB, Monclair T, Ambros PF, Brodeur GM, et al. The International Neuroblastoma Risk Group (INRG) classification system: an INRG Task Force report. J Clin Oncol 2009;27:289-97.
4. Bagatell R, Beck-Popovic M, London WB, Zhang Y, Pearson AD, Matthay KK, et al. Significance of MYCN amplification in international neuroblastoma staging system stage 1 and 2 neuroblastoma: a report from the International Neuroblastoma Risk Group database. J Clin Oncol 2009;27:365-70.
5. Canete A, Gerrard M, Rubie H, Castel V, Di Cataldo A, Munzer C, et al. Poor survival for infants with MYCN-amplified metastatic neuroblastoma despite intensified treatment: the International Society of Paediatric Oncology European Neuroblastoma Experience. J Clin Oncol 2009;27:1014-9.
6. Hurlin PJ. N-Myc functions in transcription and development. Birth Defects Res C Embryo Today 2005;75:340-52.
7. Meyer N, Penn LZ. Reflecting on 25 years with MYC. Nat Rev Cancer 2008;8:976-90.
8. Weiss WA, Aldape K, Mohapatra G, Feuerstein BG, Bishop JM. Targeted expression of MYCN causes neuroblastoma in transgenic mice. Embo J 1997;16:2985-95.
9. Nara K, Kusafuka T, Yoneda A, Oue T, Sangkhathat S, Fukuzawa M. Silencing of MYCN by RNA interference induces growth inhibition, apoptotic activity and cell differentiation in a neuroblastoma cell line with MYCN amplification. Int J Oncol 2007;30:1189-96.
10. Negroni A, Scarpa S, Romeo A, Ferrari S, Modesti A, Raschella G. Decrease of proliferation rate and induction of differentiation by a MYCN antisense DNA oligomer in a human neuroblastoma cell line. Cell Growth Differ 1991;2:511-8.
11. Burkhart CA, Cheng AJ, Madafiglio J, Kavallaris M, Mili M, Marshall GM, et al. Effects of MYCN antisense oligonucleotide administration on tumorigenesis in a murine model of neuroblastoma. J Natl Cancer Inst 2003;95:1394-403.
12. Zornig M, Busch G, Beneke R, Gulbins E, Lang F, Ma A, et al. Survival and death of prelymphomatous B-cells from N-myc/bcl-2 double transgenic mice correlates with the regulation of intracellular Ca2+ fluxes. Oncogene 1995;11:2165-74.
13. Kobayashi M, Hjerling-Leffler J, Ernfors P. Increased progenitor proliferation and apoptotic cell death in the sensory lineage of mice overexpressing N-myc. Cell Tissue Res 2006;323:81-90.
14. Tang XX, Zhao H, Kung B, Kim DY, Hicks SL, Cohn SL, et al. The MYCN enigma: significance of MYCN expression in neuroblastoma. Cancer Res 2006;66:2826-33.
15. Fulda S, Lutz W, Schwab M, Debatin KM. MycN sensitizes neuroblastoma cells for drug-induced apoptosis. Oncogene 1999;18:1479-86.
16. Lutz W, Fulda S, Jeremias I, Debatin KM, Schwab M. MycN and IFNgamma cooperate in apoptosis of human neuroblastoma cells. Oncogene 1998;17:339-46.
17. Teitz T, Wei T, Valentine MB, Vanin EF, Grenet J, Valentine VA, et al. Caspase 8 is deleted or silenced preferentially in childhood neuroblastomas with amplification of MYCN. Nat Med 2000;6:529-35. (Pubitemid 30305902)
18. van Noesel MM, Pieters R, Voute PA, Versteeg R. The N-myc paradox: N-myc overexpression in neuroblastomas is associated with sensitivity as well as resistance to apoptosis. Cancer Lett 2003;197:165-72.
19. Fulda S, Poremba C, Berwanger B, Hacker S, Eilers M, Christiansen H, et al. Loss of caspase-8 expression does not correlate with MYCN amplification, aggressive disease, or prognosis in neuroblastoma. Cancer Res 2006;66:10016-23.
20. Keshelava N, Seeger RC, Groshen S, Reynolds CP. Drug resistance patterns of human neuroblastoma cell lines derived from patients at different phases of therapy. Cancer Res 1998;58:5396-405.
21. Bell E, Premkumar R, Carr J, Lu X, Lovat PE, Kees UR, et al. The role of MYCN in the failure of MYCN amplified neuroblastoma cell lines to G1 arrest after DNA damage. Cell Cycle 2006;5:2639-47.
22. 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;101:1562-74.
23. Chen L, Iraci N, Gherardi S, Gamble LD, Wood KM, Perini G, et al. p53 is a direct transcriptional target of MYCN in neuroblastoma. Cancer Res 2010;70:1377-88.
24. Kurata K, Yanagisawa R, Ohira M, Kitagawa M, Nakagawara A, Kamijo T. Stress via p53 pathway causes apoptosis by mitochondrial Noxa upregulation in doxorubicin-treated neuroblastoma cells. Oncogene 2008;27:741-54.
25. Lutz W, Stohr M, Schurmann J, Wenzel A, Lohr A, Schwab M. 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 1996;13:803-12.
26. D'Orazi G, Cecchinelli B, Bruno T, Manni I, Higashimoto Y, Saito S, et al. Homeodomain-interacting protein kinase-2 phosphorylates p53 at Ser 46 and mediates apoptosis. Nat Cell Biol 2002;4:11-9.
27. Rinaldo C, Prodosmo A, Siepi F, Moncada A, Sacchi A, Selivanova G, et al. HIPK2 regulation by MDM2 determines tumor cell response to the p53-reactivating drugs nutlin-3 and RITA. Cancer Res 2009;69:6241-8.
28. Hematulin A, Sagan D, Eckardt-Schupp F, Moertl S. NBS1 is required for IGF-1 induced cellular proliferation through the Ras/Raf/MEK/ERK cascade. Cell Signal 2008;20:2276-85.
29. Pierantoni GM, Rinaldo C, Mottolese M, Di Benedetto A, Esposito F, Soddu S, et al. High-mobility group A1 inhibits p53 by cytoplasmic relocalization of its proapoptotic activator HIPK2. J Clin Invest 2007;117:693-702.
30. Cheng Q, Chen J. Mechanism of p53 stabilization by ATM after DNA damage. Cell Cycle 2010;9:472-8.
31. Yoshida K, Miki Y. The cell death machinery governed by the p53 tumor suppressor in response to DNA damage. Cancer Sci 2010;101:831-5.
32. Mayo LD, Seo YR, Jackson MW, Smith ML, Rivera Guzman J, Korgaonkar CK, et al. Phosphorylation of human p53 at serine 46 determines promoter selection and whether apoptosis is attenuated or amplified. J Biol Chem 2005;280:25953-9.
33. Oda K, Arakawa H, Tanaka T, Matsuda K, Tanikawa C, Mori T, et al. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell 2000;102:849-62.
34. Appella E, Anderson CW. Post-translational modifications and activation of p53 by genotoxic stresses. Eur J Biochem 2001;268:2764-72.
35. Saito S, Goodarzi AA, Higashimoto Y, Noda Y, Lees-Miller SP, Appella E, et al. ATM mediates phosphorylation at multiple p53 sites, including Ser(46), in response to ionizing radiation. J Biol Chem 2002;277:12491-4.
36. Hofmann TG, Moller A, Sirma H, Zentgraf H, Taya Y, Droge W, et al. Regulation of p53 activity by its interaction with homeodomain-interacting protein kinase-2. Nat Cell Biol 2002;4:1-10.
37. Calzado MA, de la Vega L, Moller A, Bowtell DD, Schmitz ML. An inducible autoregulatory loop between HIPK2 and Siah2 at the apex of the hypoxic response. Nat Cell Biol 2009;11:85-91.
38. Choi DW, Seo YM, Kim EA, Sung KS, Ahn JW, Park SJ, et al. Ubiquitination and degradation of homeodomain-interacting protein kinase 2 by WD40 repeat/SOCS box protein WSB-1. J Biol Chem 2008;283:4682-9.
39. Rinaldo C, Prodosmo A, Mancini F, Iacovelli S, Sacchi A, Moretti F, et al. MDM2-regulated degradation of HIPK2 prevents p53Ser46 phosphorylation and DNA damage-induced apoptosis. Mol Cell 2007;25:739-50.
40. Winter M, Sombroek D, Dauth I, Moehlenbrink J, Scheuermann K, Crone J, et al. Control of HIPK2 stability by ubiquitin ligase Siah-1 and checkpoint kinases ATM and ATR. Nat Cell Biol 2008;10:812-24.
41. Bartek J, Bartkova J, Lukas J. DNA damage signalling guards against activated oncogenes and tumour progression. Oncogene 2007;26:7773-9.
42. Tovar C, Rosinski J, Filipovic Z, Higgins B, Kolinsky K, Hilton H, et al. Small-molecule MDM2 antagonists reveal aberrant p53 signaling in cancer: implications for therapy. Proc Natl Acad Sci USA 2006;103:1888-93.
43. Tweddle DA, Pearson AD, Haber M, Norris MD, Xue C, Flemming C, et al. The p53 pathway and its inactivation in neuroblastoma. Cancer Lett 2003;197:93-8. (Pubitemid 36859996)
44. Chesler L, Goldenberg DD, Collins R, Grimmer M, Kim GE, Tihan T, et al. Chemotherapy-induced apoptosis in a transgenic model of neuroblastoma proceeds through p53 induction. Neoplasia 2008;10:1268-74.
45. Doxakis E, Huang EJ, Davies AM. Homeodomain-interacting protein kinase-2 regulates apoptosis in developing sensory and sympathetic neurons. Curr Biol 2004;14:1761-5.
46. Calzado MA, Renner F, Roscic A, Schmitz ML. HIPK2: a versatile switchboard regulating the transcription machinery and cell death. Cell Cycle 2007;6:139-43.
47. Kurihara A, Nagoshi H, Yabuki M, Okuyama R, Obinata M, Ikawa S. Ser46 phosphorylation of p53 is not always sufficient to induce apoptosis: multiple mechanisms of regulation of p53-dependent apoptosis. Genes Cells 2007;12:853-61.
48. Puca R, Nardinocchi L, Givol D, D'Orazi G. Regulation of p53 activity by HIPK2: molecular mechanisms and therapeutical implications in human cancer cells. Oncogene 2010.
49. Feng L, Hollstein M, Xu Y. Ser46 phosphorylation regulates p53-dependent apoptosis and replicative senescence. Cell Cycle 2006;5:2812-9.
50. Van Maerken T, Vandesompele J, Rihani A, De Paepe A, Speleman F. Escape from p53-mediated tumor surveillance in neuroblastoma: switching off the p14(ARF)-MDM2-p53 axis. Cell Death Differ 2009;16:1563-72.
51. Giannini G, Cerignoli F, Mellone M, Massimi I, Ambrosi C, Rinaldi C, et al. High mobility group A1 is a molecular target for MYCN in human neuroblastoma. Cancer Res 2005;65:8308-16.
52. Ventura A, Kirsch DG, McLaughlin ME, Tuveson DA, Grimm J, Lintault L, et al. Restoration of p53 function leads to tumour regression in vivo. Nature 2007;445:661-5.
53. Martins CP, Brown-Swigart L, Evan GI. Modeling the therapeutic efficacy of p53 restoration in tumors. Cell 2006;127:1323-34.
54. Xue W, Zender L, Miething C, Dickins RA, Hernando E, Krizhanovsky V, et al. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 2007;445:656-60.
55. Van Maerken T, Speleman F, Vermeulen J, Lambertz I, De Clercq S, De Smet E, et al. Small-Molecule MDM2 Antagonists as a New Therapy Concept for Neuroblastoma. Cancer Res 2006;66:9646-55.