Disruption of the MDM2-p53 interaction strongly potentiates p53-dependent apoptosis in cisplatin-resistant human testicular carcinoma cells via the Fas/FasL pathway

Cell Death and Disease

Volumn 2, Issue 4, 2011, Pages

  Koster, R ^a   Timmer Bosscha, H ^a   Bischoff, R ^b   Gietema, J A ^a   De Jong, S ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Cisplatin; Fas; MDM2; Nutlin 3; Testicular cancer; Wild type p53

Indexed keywords

CISPLATIN; FAS LIGAND; NUTLIN 3; PROTEIN MDM2; PROTEIN P53; ANTINEOPLASTIC AGENT; CDKN1A PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; FAS ANTIGEN; FAS PROTEIN, HUMAN; FASLG PROTEIN, HUMAN; IMIDAZOLE DERIVATIVE; MDM2 PROTEIN, HUMAN; PIPERAZINE DERIVATIVE; TP53 PROTEIN, HUMAN;

ACUTE GRANULOCYTIC LEUKEMIA; APOPTOSIS; ARTICLE; CARCINOMA CELL; CELL SURFACE; HODGKIN DISEASE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; TESTIS CARCINOMA; WILD TYPE; CELL SURVIVAL; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; DRUG RESISTANCE; GENETICS; IMMUNOPRECIPITATION; MALE; METABOLISM; MUTATION; PATHOLOGY; PROTEIN BINDING; PROTEIN TRANSPORT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TESTIS TUMOR; TUMOR CELL LINE; UPREGULATION;

ANTIGENS, CD95; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL SURVIVAL; CISPLATIN; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; FAS LIGAND PROTEIN; HUMANS; IMIDAZOLES; IMMUNOPRECIPITATION; MALE; MUTATION; PIPERAZINES; PROTEIN BINDING; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-MDM2; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TESTICULAR NEOPLASMS; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 79960014883     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2011.33     Document Type: Article

References (40)

1. Horwich A, Shipley J, Huddart R. Testicular germ-cell cancer. Lancet 2006; 367: 754-765. (Pubitemid 43326294)
2. Spierings DC, de Vries EG, Vellenga E, de Jong S. Loss of drug-induced activation of the CD95 apoptotic pathway in a cisplatin-resistant testicular germ cell tumor cell line. Cell Death Differ 2003; 10: 808-822. (Pubitemid 36850242)
3. Burger H, Nooter K, Boersma AW, van Wingerden KE, Looijenga LH, Jochemsen AG et al. Distinct p53-independent apoptotic cell death signalling pathways in testicular germ cell tumour cell lines. Int J Cancer 1999; 81: 620-628. (Pubitemid 29203062)
4. Walker MC, Parris CN, Masters JR. Differential sensitivities of human testicular and bladder tumor cell lines to chemotherapeutic drugs. J Natl Cancer Inst 1987; 79: 213-216. (Pubitemid 17124345)
5. di Pietro A, Vries EG, Gietema JA, Spierings DC, de Jong S. Testicular germ cell tumours: the paradigm of chemo-sensitive solid tumours. Int J Biochem Cell Biol 2005; 37: 2437-2456. (Pubitemid 41400315)
6. Johnstone RW, Ruefli AA, Lowe SW. Apoptosis: a link between cancer genetics and chemotherapy. Cell 2002; 108: 153-164. (Pubitemid 34161136)
7. Vousden KH, Prives C. Blinded by the light: the growing complexity of p53. Cell 2009; 137: 413-431.
8. Hamroun D, Kato S, Ishioka C, Claustres M, Beroud C, Soussi T. The UMD TP53 database and website: update and revisions. Hum Mutat 2006; 27: 14-20. (Pubitemid 43042962)
9. Houldsworth J, Korkola JE, Bosl GJ, Chaganti RS. Biology and genetics of adult male germ cell tumors. J Clin Oncol 2006; 24: 5512-5518. (Pubitemid 46631331)
10. Chresta CM, Arriola EL, Hickman JA. Apoptosis and cancer chemotherapy. Behring Inst Mitt 1996; 97: 232-240.
11. Houldsworth J, Xiao H, Murty VV, Chen W, Ray B, Reuter VE et al. Human male germ cell tumor resistance to cisplatin is linked to TP53 gene mutation. Oncogene 1998; 16: 2345-2349. (Pubitemid 28226881)
12. Arriola EL, Rodriguez-Lopez AM, Hickman JA, Chresta CM. Bcl-2 overexpression results in reciprocal downregulation of Bcl-X(L) and sensitizes human testicular germ cell tumours to chemotherapy-induced apoptosis. Oncogene 1999; 18: 1457-1464. (Pubitemid 29103633)
13. Kersemaekers AM, Mayer F, Molier M, van Weeren PC, Oosterhuis JW, Bokemeyer C, et al. Role of P53 and MDM2 in treatment response of human germ cell tumors. J Clin Oncol 2002; 20: 1551-1561. (Pubitemid 34260535)
14. Oliver RT, Shamash J, Berney DM. p53 and MDM2 in germ cell cancer treatment response. J Clin Oncol 2002; 20: 3928; author reply 3928-3929.
15. Kerley-Hamilton JS, Pike AM, Li N, DiRenzo J, Spinella MJ. A p53-dominant transcriptional response to cisplatin in testicular germ cell tumor-derived human embryonal carcinoma. Oncogene 2005; 24: 6090-6100. (Pubitemid 43080059)
16. Di Vizio D, Cito L, Boccia A, Chieffi P, Insabato L, Pettinato G et al. Loss of the tumor suppressor gene PTEN marks the transition from intratubular germ cell neoplasias (ITGCN) to invasive germ cell tumors. Oncogene 2005; 24: 1882-1894. (Pubitemid 40462790)
17. Datta MW, Macri E, Signoretti S, Renshaw AA, Loda M. Transition from in situ to invasive testicular germ cell neoplasia is associated with the loss of p21 and gain of mdm-2 expression. Mod Pathol 2001; 14: 437-442. (Pubitemid 32448742)
18. Voorhoeve PM, le Sage C, Schrier M, Gillis AJ, Stoop H, Nagel R et al. A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell 2006; 124: 1169-1181.
19. Koster R, di Pietro A, Timmer-Bosscha H, Gibcus JH, van den Berg A, Suurmeijer AJ et al. Cytoplasmic p21 expression levels determine cisplatin resistance in human testicular cancer. J Clin Invest 2010; 120: 3594-3605.
20. 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)
21. Kojima K, Konopleva M, Samudio IJ, Shikami M, Cabreira-Hansen M, McQueen T et al. MDM2 antagonists induce p53-dependent apoptosis in AML: implications for leukemia therapy. Blood 2005; 106: 3150-3159. (Pubitemid 41565913)
22. Janz M, Stuhmer T, Vassilev LT, Bargou RC. Pharmacologic activation of p53-dependent and p53-independent apoptotic pathways in Hodgkin/Reed-Sternberg cells. Leukemia 2007; 21: 772-779. (Pubitemid 46444562)
23. Vassilev LT. MDM2 inhibitors for cancer therapy. Trends Mol Med 2007; 13: 23-31. (Pubitemid 46027725)
24. Bauer S, Muhlenberg T, Leahy M, Hoiczyk M, Gauler T, Schuler M et al. Therapeutic potential of Mdm2 inhibition in malignant germ cell tumours. Eur Urol 2010; 57: 679-687.
25. Li B, Cheng Q, Li Z, Chen J. p53 inactivation by MDM2 and MDMX negative feedback loops in testicular germ cell tumors. Cell Cycle 2010; 9: 1411-1420.
26. Fulda S, Los M, Friesen C, Debatin KM. Chemosensitivity of solid tumor cells in vitro is related to activation of the CD95 system. Int J Cancer 1998; 76: 105-114. (Pubitemid 28164576)
27. Friesen C, Fulda S, Debatin KM. Cytotoxic drugs and the CD95 pathway. Leukemia 1999; 13: 1854-1858. (Pubitemid 29535271)
28. Timmer T, de Vries EG, de Jong S. Fas receptor-mediated apoptosis: a clinical application? J Pathol 2002; 196: 125-134. (Pubitemid 34110893)
29. Spierings DC, de Vries EG, Vellenga E, de Jong S. The attractive Achilles heel of germ cell tumours: an inherent sensitivity to apoptosis-inducing stimuli. J Pathol 2003; 200: 137-148. (Pubitemid 36748022)
30. Spierings DC, de Vries EG, Stel AJ, te Rietstap N, Vellenga E, de Jong S. Low p21Waf1/ Cip1 protein level sensitizes testicular germ cell tumor cells to Fas-mediated apoptosis. Oncogene 2004; 23: 4862-4872. (Pubitemid 38937046)
31. Lutzker SG, Levine AJ. A functionally inactive p53 protein in teratocarcinoma cells is activated by either DNA damage or cellular differentiation. Nat Med 1996; 2: 804-810. (Pubitemid 26225098)
32. Zamble DB, Jacks T, Lippard SJ. p53-dependent and -independent responses to cisplatin in mouse testicular teratocarcinoma cells. Proc Natl Acad Sci USA 1998; 95: 6163-6168. (Pubitemid 28248982)
33. Xia M, Knezevic D, Vassilev LT. p21 does not protect cancer cells from apoptosis induced by nongenotoxic p53 activation. Oncogene 2011; 30: 346-355.
34. Espinosa JM, Verdun RE, Emerson BM. p53 functions through stress- and promoterspecific recruitment of transcription initiation components before and after DNA damage. Mol Cell 2003; 12: 1015-1027. (Pubitemid 37352792)
35. Gomes NP, Espinosa JM. Differential regulation of p53 target genes: it's (core promoter) elementary. Genes Dev 2010; 24: 111-114.
36. Morachis JM, Murawsky CM, Emerson BM. Regulation of the p53 transcriptional response by structurally diverse core promoters. Genes Dev 2010; 24: 135-147.
37. Jiang M, Pabla N, Murphy RF, Yang T, Yin XM, Degenhardt K et al. Nutlin-3 protects kidney cells during cisplatin therapy by suppressing Bax/Bak activation. J Biol Chem 2007; 282: 2636-2645. (Pubitemid 47076791)
38. Timmer-Bosscha H, Timmer A, Meijer C, de Vries EG, de Jong B, Oosterhuis JW et al. cisdiamminedichloroplatinum( ii) resistance in vitro and in vivo in human embryonal carcinoma cells. Cancer Res 1993; 53: 5707-5713.
39. Sark MW, Timmer-Bosscha H, Meijer C, Uges DR, Sluiter WJ, Peters WH et al. Cellular basis for differential sensitivity to cisplatin in human germ cell tumour and colon carcinoma cell lines. Br J Cancer 1995; 71: 684-690.
40. Timmer-Bosscha H, de Vries EG, Meijer C, Oosterhuis JW, Mulder NH. Differential effects of all-trans-retinoic acid, docosahexaenoic acid, and hexadecylphosphocholine on cisplatin-induced cytotoxicity and apoptosis in a cisplantin-sensitive and resistant human embryonal carcinoma cell line. Cancer Chemother Pharmacol 1998; 41: 469-476. (Pubitemid 28140711)