Escape from p53-mediated tumor surveillance in neuroblastoma: Switching off the p14ARF-MDM2-p53 axis

Cell Death and Differentiation

Volumn 16, Issue 12, 2009, Pages 1563-1572

  Van Maerken, T ^a   Vandesompele, J ^a   Rihani, A ^a   De Paepe, A ^a   Speleman, F ^a  

^a GHENT UNIVERSITY HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BMI1 PROTEIN; CHD5 PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; MYC PROTEIN; ONCOPROTEIN; PPM1D PROTEIN; PROTEIN MDM2; PROTEIN P53; TRANSCRIPTION FACTOR TWIST; TRANSCRIPTION FACTOR TWIST1; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

AUTOREGULATION; CARCINOGENESIS; CELLULAR DISTRIBUTION; CHROMOSOME 17; CYTOPLASM; GENE INACTIVATION; GENE REPRESSION; HUMAN; MALIGNANT TRANSFORMATION; NEUROBLASTOMA; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGNOSIS; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSACTIVATION; TRANSCRIPTION REGULATION; UBIQUITINATION;

ANIMALS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEUROBLASTOMA; PROTO-ONCOGENE PROTEINS C-MDM2; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P14ARF; TUMOR SUPPRESSOR PROTEIN P53;

EID: 70449712606     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2009.138     Document Type: Review

References (145)

1. 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: 93-98.
2. Tweddle DA, Malcolm AJ, Bown N, Pearson AD, Lunec J. Evidence for the development of p53 mutations after cytotoxic therapy in a neuroblastoma cell line. Cancer Res 2001; 61: 8-13.
3. Kotchetkov R, Driever PH, Cinatl J, Michaelis M, Karaskova J, Blaheta R et al. Increased malignant behavior in neuroblastoma cells with acquired multi-drug resistance does not depend on P-gp expression. Int J Oncol 2005; 27: 1029-1037.
4. Xue C, Haber M, Flemming C, Marshall GM, Lock RB, MacKenzie KL et al p53 determines multidrug sensitivity of childhood neuroblastoma. Cancer Res 2007; 67: 10351-10360.
5. Keshelava N, Zuo JJ, Chen P, Waidyaratne SN, Luna MC, Gomer CJ et al Loss of p53 function confers high-level multidrug resistance in neuroblastoma cell lines. Cancer Res 2001; 61: 6185-6193.
6. ARF pathway in neuroblastoma cell lines established at relapse. Cancer Res 2006; 66: 2138-2145.
7. Goldman SC, Chen CY, Lansing TJ, Gilmer TM, Kastan MB. The p53 signal transduction pathway is intact in human neuroblastoma despite cytoplasmic localization. Am J Pathol 1996; 148: 1381-1385.
8. 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: 9646-9655.
9. Chen L, Malcolm AJ, Wood KM, Cole M, Variend S, Cullinane C et al. p53 is nuclear and functional in both undifferentiated and differentiated neuroblastoma. Cell Cycle 2007; 6: 2685-2696.
10. Cahilly-Snyder L, Yang-Feng T, Francke U, George DL. Molecular analysis and chromosomal mapping of amplified genes isolated from a transformed mouse 3T3 cell line. Somat Cell Mol Genet 1987; 13: 235-244.
11. Marine JC, Francoz S, Maetens M, Wahl G, Toledo F, Lozano G. Keeping p53 in check: Essential and synergistic functions of Mdm2 and Mdm4. Cell Death Differ 2006; 13: 927-934.
12. Vousden KH, Lu X. Live or let die: The cell's response to p53. Nat Rev Cancer 2002; 2: 594-604.
13. Oliner JD, Pietenpol JA, Thiagalingam S, Gyuris J, Kinzler KW, Vogelstein B. Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53. Nature 1993; 362: 857-860.
14. Thut CJ, Goodrich JA, Tjian R. Repression of p53-mediated transcription by MDM2: A dual mechanism. Genes Dev 1997; 11: 1974-1986.
15. Wadgaonkar R, Collins T. Murine double minute (MDM2) blocks p53-coactivator interaction, a new mechanism for inhibition of p53-dependent gene expression. J Biol Chem 1999; 274: 13760-13767.
16. Kohn KW, Pommier Y. Molecular interaction map of the p53 and Mdm2 logic elements, which control the Off On switch of p53 in response to DNA damage. Biochem Biophys Res Commun 2005; 331: 816-827.
17. Brooks CL, Gu W. p53 ubiquitination: Mdm2 and beyond. Mol Cell 2006; 21: 307-315.
18. Minsky N, Oren M. The RING domain of Mdm2 mediates histone ubiquitylation and transcriptional repression. Mol Cell 2004; 16: 631-639.
19. Xirodimas DP, Saville MK, Bourdon JC, Hay RT, Lane DP. Mdm2-mediated NEDD8 conjugation of p53 inhibits its transcriptional activity. Cell 2004; 118: 83-97.
20. Ito A, Kawaguchi Y, Lai CH, Kovacs JJ, Higashimoto Y, Appella E et al MDM2-HDAC1-mediated deacetylation of p53 is required for its degradation. EMBO J 2002; 21: 6236-6245.
21. Mirnezami AH, Campbell SJ, Darley M, Primrose JN, Johnson PW, Blaydes JP. Hdm2 recruits a hypoxia-sensitive corepressor to negatively regulate p53-dependent transcription. Curr Biol 2003; 13: 1234-1239.
22. Sui G, Affar el B, Shi Y, Brignone C, Wall NR, Yin P et al. Yin Yang 1 is a negative regulator of p53. Cell 2004; 117: 859-872.
23. Wang C, Ivanov A, Chen L, Fredericks WJ, Seto E, Rauscher 3rd FJ et al. MDM2 interaction with nuclear corepressor KAP1 contributes to p53 inactivation. EMBO J 2005; 24: 3279-3290.
24. Lowe SW, Sherr CJ. Tumor suppression by Ink4a-Arf: Progress and puzzles. Curr Opin Genet Dev 2003; 13: 77-83.
25. Sherr CJ. Divorcing ARF and p53: An unsettled case. Nat Rev Cancer 2006; 6: 663-673.
26. Efeyan A, Garcia-Cao I, Herranz D, Velasco-Miguel S, Serrano M. Tumour biology: Policing of oncogene activity by p53. Nature 2006; 443 159.
27. Christophorou MA, Ringshausen I, Finch AJ, Swigart LB, Evan GI. The pathological response to DNA damage does not contribute to p53-mediated tumour suppression. Nature 2006; 443: 214-217.
28. ARF with Mdm2 inhibits ubiquitin ligase activity of Mdm2 for tumor suppressor p53. EMBO J 1999; 18: 22-27.
29. Zhang Y, Xiong Y. Mutations in human ARF exon 2 disrupt its nucleolar localization and impair its ability to block nuclear export of MDM2 and p53. Mol Cell 1999; 3: 579-591.
30. ARF stabilizes p53 by blocking nucleo-cytoplasmic shuttling of Mdm2. Proc Natl Acad Sci USA 1999; 96: 6937-6941.
31. Weber JD, Taylor LJ, Roussel MF, Sherr CJ, Bar-Sagi D. Nucleolar Arf sequesters Mdm2 and activates p53. Nat Cell Biol 1999; 1: 20-26.
32. ARF peptide blocks Mdm2-dependent ubiquitination in vitro and can activate p53 in vivo. Oncogene 2000; 19 2312-2323.
33. Lin AW, Lowe SW. Oncogenic ras activates the ARF-p53 pathway to suppress epithelial cell transformation. Proc Natl Acad Sci USA 2001; 98: 5025-5030.
34. ARF without relocation of MDM2 to the nucleolus. Nat Cell Biol 2001; 3: 445-452.
35. Korgaonkar C, Hagen J, Tompkins V, Frazier AA, Allamargot C, Quelle FW et al. Nucleophosmin (B23) targets ARF to nucleoli and inhibits its function. Mol Cell Biol 2005; 25: 1258-1271.
36. Gjerset RA, Bandyopadhyay K. Regulation of p14ARF through subnuclear compartmentalization. Cell Cycle 2006; 5: 686-690.
37. Chen D, Kon N, Li M, Zhang W, Qin J, Gu W. ARF-BP1/Mule is a critical mediator of the ARF tumor suppressor. Cell 2005; 121: 1071-1083.
38. Rocha S, Campbell KJ, Perkins ND. p53- and Mdm2-independent repression of NF-κB transactivation by the ARF tumor suppressor. Mol Cell 2003; 12: 15-25.
39. Corvi R, Savelyeva L, Amler L, Handgretinger R, Schwab M. Cytogenetic evolution of MYCN and MDM2 amplification in the neuroblastoma LS tumour and its cell line. Eur J Cancer 1995; 31A: 520-523.
40. Corvi R, Savelyeva L, Breit S, Wenzel A, Handgretinger R, Barak J et al. Non-syntenic amplification of MDM2 and MYCN in human neuroblastoma. Oncogene 1995; 10: 1081-1086.
41. Van Roy N, Forus A, Myklebost O, Cheng NC, Versteeg R, Speleman F. Identification of two distinct chromosome 12-derived amplification units in neuroblastoma cell line NGP. Cancer Genet Cytogenet 1995; 82 151-154.
42. 1 checkpoint function is attenuated. Clin Cancer Res 1999; 5: 4199-4207.
43. 1 arrest despite WAF1 induction in MYCN-amplified cells. Am J Pathol 2001; 158: 2067-2077.
44. ARF) but not within 1p36 or at other tumor suppressor loci in neuroblastoma. Cancer Res 2001; 61: 679-686.
45. Caren H, Erichsen J, Olsson L, Enerback C, Sjoberg RM, Abrahamsson J et al. Highresolution array copy number analyses for detection of deletion, gain, amplification and copy-neutral LOH in primary neuroblastoma tumors: Four cases of homozygous deletions of the CDKN2A gene. BMC Genomics 2008; 9: 353.
46. Takita J, Hayashi Y, Kohno T, Yamaguchi N, Hanada R, Yamamoto K et al Deletion map of chromosome 9 and p16 (CDKN2A) gene alterations in neuroblastoma. Cancer Res 1997; 57: 907-912.
47. Takita J, Hayashi Y, Nakajima T, Adachi J, Tanaka T, Yamaguchi N et al. The p16 (CDKN2A) gene is involved in the growth of neuroblastoma cells and its expression is associated with prognosis of neuroblastoma patients. Oncogene 1998; 17: 3137-3143.
48. Bond GL, Hu W, Bond EE, Robins H, Lutzker SG, Arva NC et al. A single nucleotide polymorphism in the MDM2 promoter attenuates the p53 tumor suppressor pathway and accelerates tumor formation in humans. Cell 2004; 119: 591-602.
49. Cattelani S, Defferrari R, Marsilio S, Bussolari R, Candini O, Corradini F et al. Impact of a single nucleotide polymorphism in the MDM2 gene on neuroblastoma development and aggressiveness: Results of a pilot study on 239 patients. Clin Cancer Res 2008; 14: 3248-3253.
50. Perfumo C, Parodi S, Mazzocco K, Defferrari R, Inga A, Haupt R et al Impact of MDM2 SNP309 genotype on progression and survival of stage 4 neuroblastoma. Eur J Cancer 2008; 44: 2634-2639.
51. Brodeur GM. Neuroblastoma: Biological insights into a clinical enigma. Nat Rev Cancer 2003; 3: 203-216.
52. Brodeur GM, Seeger RC, Schwab M, Varmus HE, Bishop JM. Amplification of N-myc in untreated human neuroblastomas correlates with advanced disease stage. Science 1984; 224: 1121-1124.
53. Seeger RC, Brodeur GM, Sather H, Dalton A, Siegel SE, Wong KY et al Association of multiple copies of the N-myc oncogene with rapid progression of neuroblastomas. N Engl J Med 1985; 313: 1111-1116.
54. Wenzel A, Schwab M. The mycN/max protein complex in neuroblastoma. Short review. Eur J Cancer 1995; 31A: 516-519.
55. Schwab M, Varmus HE, Bishop JM. Human N-myc gene contributes to neoplastic transformation of mammalian cells in culture. Nature 1985; 316: 160-162.
56. Small MB, Hay N, Schwab M, Bishop JM. Neoplastic transformation by the human gene N-myc. Mol Cell Biol 1987; 7: 1638-1645.
57. Schweigerer L, Breit S, Wenzel A, Tsunamoto K, Ludwig R, Schwab M. Augmented MYCN expression advances the malignant phenotype of human neuroblastoma cells: Evidence for induction of autocrine growth factor activity. Cancer Res 1990; 50: 4411-4416.
58. Lutz W, Stohr M, Schurmann J, Wenzel A, Lohr A, Schwab M. Conditional expression of N-myc in human neuroblastoma cells increases expression of α-prothymosin and ornithine decarboxylase and accelerates progression into S-phase early after mitogenic stimulation of quiescent cells. Oncogene 1996; 13: 803-812.
59. Goodman LA, Liu BC, Thiele CJ, Schmidt ML, Cohn SL, Yamashiro JM et al. Modulation of N-myc expression alters the invasiveness of neuroblastoma. Clin Exp Metastasis 1997; 15: 130-139.
60. Sugihara E, Kanai M, Matsui A, Onodera M, Schwab M, Miwa M. Enhanced expression of MYCN leads to centrosome hyperamplification after DNA damage in neuroblastoma cells. Oncogene 2004; 23: 1005-1009.
61. Slack AD, Chen Z, Ludwig AD, Hicks J, Shohet JM. MYCN-directed centrosome amplification requires MDM2-mediated suppression of p53 activity in neuroblastoma cells. Cancer Res 2007; 67: 2448-2455.
62. Fotsis T, Breit S, Lutz W, Rossler J, Hatzi E, Schwab M et al. Down-regulation of endothelial cell growth inhibitors by enhanced MYCN oncogene expression in human neuroblastoma cells. Eur J Biochem 1999; 263: 757-764.
63. Hatzi E, Breit S, Zoephel A, Ashman K, Tontsch U, Ahorn H et al. MYCN oncogene and angiogenesis: Down-regulation of endothelial growth inhibitors in human neuroblastoma cells. Purification, structural, and functional characterization. Adv Exp Med Biol 2000; 476: 239-248.
64. Song L, Ara T, Wu HW, Woo CW, Reynolds CP, Seeger RC et al. Oncogene MYCN regulates localization of NKT cells to the site of disease in neuroblastoma. J Clin Invest 2007; 117: 2702-2712.
65. Weiss WA, Aldape K, Mohapatra G, Feuerstein BG, Bishop JM. Targeted expression of MYCN causes neuroblastoma in transgenic mice. EMBO J 1997; 16: 2985-2995.
66. Lutz W, Fulda S, Jeremias I, Debatin KM, Schwab M. MycN and IFNγ cooperate in apoptosis of human neuroblastoma cells. Oncogene 1998; 17: 339-346.
67. Fulda S, Lutz W, Schwab M, Debatin KM. MycN sensitizes neuroblastoma cells for drug-induced apoptosis. Oncogene 1999; 18: 1479-1486.
68. Fulda S, Lutz W, Schwab M, Debatin KM. MycN sensitizes neuroblastoma cells for drug-triggered apoptosis. Med Pediatr Oncol 2000; 35 582-584.
69. van Golen CM, Soules ME, Grauman AR, Feldman EL. N-Myc overexpression leads to decreased β1 integrin expression and increased apoptosis in human neuroblastoma cells. Oncogene 2003; 22: 2664-2673.
70. Slack A, Chen Z, Tonelli R, Pule M, Hunt L, Pession A et al. The p53 regulatory gene MDM2 is a direct transcriptional target of MYCN in neuroblastoma. Proc Natl Acad Sci USA 2005; 102: 731-736.
71. Alt JR, Greiner TC, Cleveland JL, Eischen CM. Mdm2 haplo-insufficiency profoundly inhibits Myc-induced lymphomagenesis. EMBO J 2003; 22: 1442-1450.
72. Firulli AB, Conway SJ. Phosphoregulation of Twist1 provides a mechanism of cell fate control. Curr Med Chem 2008; 15: 2641-2647.
73. Howard TD, Paznekas WA, Green ED, Chiang LC, Ma N, Ortiz de Luna RI et al. Mutations in TWIST, a basic helix-loop-helix transcription factor, in Saethre-Chotzen syndrome. Nat Genet 1997; 15: 36-41.
74. el Ghouzzi V, Le Merrer M, Perrin-Schmitt F, Lajeunie E, Benit P, Renier D et al. Mutations of the TWIST gene in the Saethre-Chotzen syndrome. Nat Genet 1997; 15: 42-46.
75. Valsesia-Wittmann S, Magdeleine M, Dupasquier S, Garin E, Jallas AC, Combaret V et al. Oncogenic cooperation between H-Twist and N-Myc overrides failsafe programs in cancer cells. Cancer Cell 2004; 6: 625-630.
76. Maestro R, Dei Tos AP, Hamamori Y, Krasnokutsky S, Sartorelli V, Kedes L et al. twist is a potential oncogene that inhibits apoptosis. Genes Dev 1999; 13: 2207-2217.
77. Hamamori Y, Sartorelli V, Ogryzko V, Puri PL, Wu HY, Wang JY et al Regulation of histone acetyltransferases p300 and PCAF by the bHLH protein twist and adenoviral oncoprotein E1A. Cell 1999; 96: 405-413.
78. Stasinopoulos IA, Mironchik Y, Raman A, Wildes F, Winnard Jr P, Raman V. HOXA5-twist interaction alters p53 homeostasis in breast cancer cells. J Biol Chem 2005; 280: 2294-2299.
79. Shiota M, Izumi H, Onitsuka T, Miyamoto N, Kashiwagi E, Kidani A et al. Twist and p53 reciprocally regulate target genes via direct interaction. Oncogene 2008; 27: 5543-5553.
80. Ansieau S, Bastid J, Doreau A, Morel AP, Bouchet BP, Thomas C et al Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell 2008; 14: 79-89.
81. Nowak K, Kerl K, Fehr D, Kramps C, Gessner C, Killmer K et al. BMI1 is a target gene of E2F-1 and is strongly expressed in primary neuroblastomas. Nucleic Acids Res 2006; 34: 1745-1754.
82. Cui H, Hu B, Li T, Ma J, Alam G, Gunning WT et al. Bmi-1 is essential for the tumorigenicity of neuroblastoma cells. Am J Pathol 2007; 170: 1370-1378.
83. Sparmann A, van Lohuizen M. Polycomb silencers control cell fate, development and cancer. Nat Rev Cancer 2006; 6: 846-856.
84. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 1999; 397: 164-168.
85. Lessard J, Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 2003; 423 255-260.
86. Park IK, Qian D, Kiel M, Becker MW, Pihalja M, Weissman IL et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 2003; 423: 302-305.
87. Molofsky AV, Pardal R, Iwashita T, Park IK, Clarke MF, Morrison SJ. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 2003; 425: 962-967.
88. Arf senescence pathways. Genes Dev 2005; 19: 1432-1437.
89. van Lohuizen M, Verbeek S, Scheijen B, Wientjens E, van der Gulden H, Berns A. Identification of cooperating oncogenes in Em-myc transgenic mice by provirus tagging. Cell 1991; 65: 737-752.
90. Haupt Y, Alexander WS, Barri G, Klinken SP, Adams JM. Novel zinc finger gene implicated as myc collaborator by retrovirally accelerated lymphomagenesis in μ-myc transgenic mice. Cell 1991; 65 753-763.
91. Haupt Y, Bath ML, Harris AW, Adams JM. bmi-1 transgene induces lymphomas and collaborates with myc in tumorigenesis. Oncogene 1993; 8: 3161-3164.
92. Alkema MJ, Jacobs H, van Lohuizen M, Berns A. Pertubation of B and T cell development and predisposition to lymphomagenesis in EμBmi1 transgenic mice require the Bmi1 RING finger. Oncogene 1997; 15 899-910.
93. Jacobs JJ, Scheijen B, Voncken JW, Kieboom K, Berns A, van Lohuizen M. Bmi-1 collaborates with c-Myc in tumorigenesis by inhibiting c-Myc-induced apoptosis via INK4a/ARF. Genes Dev 1999; 13: 2678-2690.
94. Datta S, Hoenerhoff MJ, Bommi P, Sainger R, Guo WJ, Dimri M et al. Bmi-1 cooperates with H-Ras to transform human mammary epithelial cells via dysregulation of multiple growth-regulatory pathways. Cancer Res 2007; 67: 10286-10295.
95. Hernando E, Nahle Z, Juan G, Diaz-Rodriguez E, Alaminos M, Hemann M et al. Rb inactivation promotes genomic instability by uncoupling cell cycle progression from mitotic control. Nature 2004; 430 797-802.
96. Strieder V, Lutz W. E2F proteins regulate MYCN expression in neuroblastomas. J Biol Chem 2003; 278: 2983-2989.
97. Cui H, Ma J, Ding J, Li T, Alam G, Ding HF. Bmi-1 regulates the differentiation and clonogenic self-renewal of I-type neuroblastoma cells in a concentration-dependent manner. J Biol Chem 2006; 281: 34696-34704.
98. White PS, Thompson PM, Gotoh T, Okawa ER, Igarashi J, Kok M et al. Definition and characterization of a region of 1p36.3 consistently deleted in neuroblastoma. Oncogene 2005; 24: 2684-2694.
99. Okawa ER, Gotoh T, Manne J, Igarashi J, Fujita T, Silverman KA et al Expression and sequence analysis of candidates for the 1p36.31 tumor suppressor gene deleted in neuroblastomas. Oncogene 2008; 27 803-810.
100. Fujita T, Igarashi J, Okawa ER, Gotoh T, Manne J, Kolla V et al. CHD5, a tumor suppressor gene deleted from 1p36.31 in neuroblastomas. J Natl Cancer Inst 2008; 100: 940-949.
101. Thompson PM, Gotoh T, Kok M, White PS, Brodeur GM. CHD5, a new member of the chromodomain gene family, is preferentially expressed in the nervous system. Oncogene 2003; 22: 1002-1011.
102. Bagchi A, Papazoglu C, Wu Y, Capurso D, Brodt M, Francis D et al. CHD5 is a tumor suppressor at human 1p36. Cell 2007; 128: 459-475.
103. Bown N, Cotterill S, Lastowska M, O'Neill S, Pearson AD, Plantaz D et al. Gain of chromosome arm 17q and adverse outcome in patients with neuroblastoma. N Engl J Med 1999; 340: 1954-1961.
104. Vandesompele J, Baudis M, De Preter K, Van Roy N, Ambros P, Bown N et al. Unequivocal delineation of clinicogenetic subgroups and development of a new model for improved outcome prediction in neuroblastoma. J Clin Oncol 2005; 23: 2280-2299.
105. Saito-Ohara F, Imoto I, Inoue J, Hosoi H, Nakagawara A, Sugimoto T et al. PPM1D is a potential target for 17q gain in neuroblastoma. Cancer Res 2003; 63: 1876-1883.
106. Li J, Yang Y, Peng Y, Austin RJ, van Eyndhoven WG, Nguyen KC et al Oncogenic properties of PPM1D located within a breast cancer amplification epicenter at 17q23. Nat Genet 2002; 31: 133-134.
107. Bulavin DV, Demidov ON, Saito S, Kauraniemi P, Phillips C, Amundson SA et al. Amplification of PPM1D in human tumors abrogates p53 tumor-suppressor activity. Nat Genet 2002; 31: 210-215.
108. Rauta J, Alarmo EL, Kauraniemi P, Karhu R, Kuukasjarvi T, Kallioniemi A. The serine-threonine protein phosphatase PPM1D is frequently activated through amplification in aggressive primary breast tumours. Breast Cancer Res Treat 2006; 95: 257-263.
109. Hirasawa A, Saito-Ohara F, Inoue J, Aoki D, Susumu N, Yokoyama T et al. Association of 17q21-q24 gain in ovarian clear cell adenocarcinomas with poor prognosis and identification of PPM1D and APPBP2 as likely amplification targets. Clin Cancer Res 2003; 9: 1995-2004.
110. Mendrzyk F, Radlwimmer B, Joos S, Kokocinski F, Benner A, Stange DE et al. Genomic and protein expression profiling identifies CDK6 as novel independent prognostic marker in medulloblastoma. J Clin Oncol 2005; 23: 8853-8862.
111. Castellino RC, De Bortoli M, Lu X, Moon SH, Nguyen TA, Shepard MA et al. Medulloblastomas overexpress the p53-inactivating oncogene WIP1/PPM1D. J Neurooncol 2008; 86: 245-256.
112. Fiscella M, Zhang H, Fan S, Sakaguchi K, Shen S, Mercer WE et al. Wip1, a novel human protein phosphatase that is induced in response to ionizing radiation in a p53-dependent manner. Proc Natl Acad Sci USA 1997; 94: 6048-6053.
113. Takekawa M, Adachi M, Nakahata A, Nakayama I, Itoh F, Tsukuda H et al p53-inducible Wip1 phosphatase mediates a negative feedback regulation of p38 MAPK-p53 signaling in response to UV radiation. EMBO J 2000; 19: 6517-6526.
114. Lu X, Nannenga B, Donehower LA. PPM1D dephosphorylates Chk1 and p53 and abrogates cell cycle checkpoints. Genes Dev 2005; 19: 1162-1174.
115. Fujimoto H, Onishi N, Kato N, Takekawa M, Xu XZ, Kosugi A et al. Regulation of the antioncogenic Chk2 kinase by the oncogenic Wip1 phosphatase. Cell Death Differ 2006; 13: 1170-1180.
116. Yoda A, Xu XZ, Onishi N, Toyoshima K, Fujimoto H, Kato N et al. Intrinsic kinase activity and SQ/TQ domain of Chk2 kinase as well as N-terminal domain of Wip1 phosphatase are required for regulation of Chk2 by Wip1. J Biol Chem 2006; 281: 24847-24862.
117. Oliva-Trastoy M, Berthonaud V, Chevalier A, Ducrot C, Marsolier-Kergoat MC, Mann C et al. The Wip1 phosphatase (PPM1D) antagonizes activation of the Chk2 tumour suppressor kinase. Oncogene 2007; 26: 1449-1458.
118. Shreeram S, Demidov ON, Hee WK, Yamaguchi H, Onishi N, Kek C et al Wip1 phosphatase modulates ATM-dependent signaling pathways. Mol Cell 2006; 23: 757-764.
119. Shreeram S, Hee WK, Demidov ON, Kek C, Yamaguchi H, Fornace Jr AJ et al. Regulation of ATM/p53-dependent suppression of myc-induced lymphomas by Wip1 phosphatase. J Exp Med 2006; 203: 2793-2799.
120. Yamaguchi H, Durell SR, Chatterjee DK, Anderson CW, Appella E. The Wip1 phosphatase PPM1D dephosphorylates SQ/TQ motifs in checkpoint substrates phosphorylated by PI3K-like kinases. Biochemistry 2007; 46: 12594-12603.
121. Lu X, Ma O, Nguyen TA, Jones SN, Oren M, Donehower LA. The Wip1 phosphatase acts as a gatekeeper in the p53-Mdm2 autoregulatory loop. Cancer Cell 2007; 12: 342-354.
122. Arf pathway. Nat Genet 2004; 36: 343-350.
123. Nannenga B, Lu X, Dumble M, Van Maanen M, Nguyen TA, Sutton R et al Augmented cancer resistance and DNA damage response phenotypes in PPM1D null mice. Mol Carcinog 2006; 45: 594-604.
124. Demidov ON, Kek C, Shreeram S, Timofeev O, Fornace AJ, Appella E et al. The role of the MKK6/p38 MAPK pathway in Wip1-dependent regulation of ErbB2-driven mammary gland tumorigenesis. Oncogene 2007; 26: 2502-2506.
125. Moll UM, LaQuaglia M, Benard J, Riou G. Wild-type p53 protein undergoes cytoplasmic sequestration in undifferentiated neuroblastomas but not in differentiated tumors. Proc Natl Acad Sci USA 1995; 92: 4407-4411.
126. Wolff A, Technau A, Ihling C, Technau-Ihling K, Erber R, Bosch FX et al. Evidence that wild-type p53 in neuroblastoma cells is in a conformation refractory to integration into the transcriptional complex. Oncogene 2001; 20: 1307-1317.
127. Moll UM, Ostermeyer AG, Haladay R, Winkfield B, Frazier M, Zambetti G. Cytoplasmic sequestration of wild-type p53 protein impairs the G1 checkpoint after DNA damage. Mol Cell Biol 1996; 16: 1126-1137.
128. Nikolaev AY, Li M, Puskas N, Qin J, Gu W. Parc: A cytoplasmic anchor for p53. Cell 2003; 112: 29-40.
129. 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.
130. Becker K, Marchenko ND, Maurice M, Moll UM. Hyperubiquitylation of wild-type p53 contributes to cytoplasmic sequestration in neuroblastoma. Cell Death Differ 2007; 14: 1350-1360.
131. Rodriguez-Lopez AM, Xenaki D, Eden TO, Hickman JA, Chresta CM. MDM2 mediated nuclear exclusion of p53 attenuates etoposide-induced apoptosis in neuroblastoma cells. Mol Pharmacol 2001; 59: 135-143.
132. Wang X, Zalcenstein A, Oren M. Nitric oxide promotes p53 nuclear retention and sensitizes neuroblastoma cells to apoptosis by ionizing radiation. Cell Death Differ 2003m; 10: 468-476.
133. Stommel JM, Marchenko ND, Jimenez GS, Moll UM, Hope TJ, Wahl GM. A leucine-rich nuclear export signal in the p53 tetramerization domain: regulation of subcellular localization and p53 activity by NES masking. EMBO J 1999; 18: 1660-1672.
134. Lu W, Pochampally R, Chen L, Traidej M, Wang Y, Chen J. Nuclear exclusion of p53 in subset of tumors requires MDM2 function. Oncogene 2000; 19: 232-240.
135. Flaegstad T, Andresen PA, Johnsen JI, Asomani SK, Jorgensen GE, Vignarajan S et al. A possible contributory role of BK virus infection in neuroblastoma development. Cancer Res 1999; 59: 1160-1163.
136. Jorgensen GE, Johnsen JI, Ponthan F, Kogner P, Flaegstad T, Traavik T. Human polyomavirus BK (BKV) and neuroblastoma: Mechanisms of oncogenic action and possible strategy for novel treatment. Med Pediatr Oncol 2000; 35: 593-596.
137. Sengupta S, Vonesch JL, Waltzinger C, Zheng H, Wasylyk B. Negative cross-talk between p53 and the glucocorticoid receptor and its role in neuroblastoma cells. EMBO J 2000; 19: 6051-6064.
138. Ohtsubo C, Shiokawa D, Kodama M, Gaiddon C, Nakagama H, Jochemsen AG et Cytoplasmic tethering is involved in synergistic inhibition of p53 by Mdmx and Mdm2. Cancer Sci 2009; 100: 1291-1299.
139. Zaika A, Marchenko N, Moll UM. Cytoplasmically 'sequestered' wild type p53 protein is resistant to Mdm2-mediated degradation. J Biol Chem 1999; 274: 27474-27480.
140. Chen Z, Lin Y, Barbieri E, Burlingame S, Hicks J, Ludwig A et al. Mdm2 deficiency suppresses MYCN-driven neuroblastoma tumorigenesis in vivo. Neoplasia 2009; 11: 753-762.
141. Zindy F, Eischen CM, Randle DH, Kamijo T, Cleveland JL, Sherr CJ et al. Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev 1998; 12 2424-2433.
142. Aslanian A, Iaquinta PJ, Verona R, Lees JA. Repression of the Arf tumor suppressor E2F3 is required for normal cell cycle kinetics. Genes Dev 2004; 18: 1413-1422.
143. ARF gene expression. EMBO J 2005; 24: 3724-3736.
144. Barbieri E, Mehta P, Chen Z, Zhang L, Slack A, Berg S et al. MDM2 inhibition sensitizes neuroblastoma to chemotherapy-induced apoptotic cell death. Mol Cancer Ther 2006;5: 2358-2365.
145. 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 (in press).