Reactivation of p53 function in synovial sarcoma cells by inhibition of p53-HDM2 interaction

Cancer Letters

Volumn 275, Issue 2, 2009, Pages 285-292

  D'Arcy, Pádraig ^a,b   Ryan, Bríd Ann ^b   Brodin, Bertha ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b DUBLIN INSTITUTE OF TECHNOLOGY   (Ireland)

Author keywords

HDM2; Nutlin 3; p53; SS18 SSX; Synovial sarcoma

Indexed keywords

DOXORUBICIN; NUTLIN 3; PROTEIN MDM2; PROTEIN P21; PROTEIN P53;

APOPTOSIS; ARTICLE; CELL GROWTH; COMPLEX FORMATION; CONTROLLED STUDY; DNA DAMAGE; DRUG POTENTIATION; GENOTOXICITY; GROWTH INHIBITION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SYNOVIAL SARCOMA; TRANSCRIPTION INITIATION;

AMINO ACID SEQUENCE; BLOTTING, WESTERN; CELL LINE, TUMOR; DNA DAMAGE; DOXORUBICIN; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENES, P53; HUMANS; IMIDAZOLES; IMMUNOPRECIPITATION; MOLECULAR SEQUENCE DATA; ONCOGENE PROTEIN P21(RAS); PIPERAZINES; PROTO-ONCOGENE PROTEINS C-MDM2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SARCOMA, SYNOVIAL;

EID: 59349107039     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2008.10.030     Document Type: Article

References (36)

1. Vousden K.H., and Lu X. Live or let die: the cell's response to p53. Nat. Rev. Cancer 2 (2002) 594-604
2. Honda R., Tanaka H., and Yasuda H. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 420 (1997) 25-27
3. Boyd S.D., Tsai K.Y., and Jacks T. An intact HDM2 RING-finger domain is required for nuclear exclusion of p53. Nat. Cell Biol. 2 (2000) 563-568
4. Momand J., Zambetti G.P., Olson D.C., George D., and Levine A.J. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 69 (1992) 1237-1245
5. Oliner J.D., Pietenpol J.A., Thiagalingam S., Gyuris J., Kinzler K.W., and Vogelstein B. Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53. Nature 362 (1993) 857-860
6. Picksley S.M., and Lane D.P. The p53-mdm2 autoregulatory feedback loop: a paradigm for the regulation of growth control by p53?. Bioessays 15 (1993) 689-690
7. Vassilev L.T., Vu B.T., Graves B., Carvajal D., Podlaski F., Filipovic Z., Kong N., Kammlott U., Lukacs C., Klein C., Fotouhi N., and Liu E.A. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303 (2004) 844-848
8. Muller C.R., Paulsen E.B., Noordhuis P., Pedeutour F., Saeter G., and Myklebost O. Potential for treatment of liposarcomas with the MDM2 antagonist nutlin-3A. Int. J. Cancer 121 (2007) 199-205
9. Vassilev L.T., Vu B.T., Graves B., Carvajal D., Podlaski F., Filipovic Z., Kong N., Kammlott U., Lukacs C., Klein C., Fotouhi N., and Liu E.A. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303 (2004) 844-848
10. Van Maerken T., Speleman F., Vermeulen J., Lambertz I., De Clercq S., De Smet E., Yigit N., Coppens V., Philippe J., De Paepe A., Marine J.-C., and Vandesompele J. Small-molecule MDM2 antagonists as a new therapy concept for neuroblastoma. Cancer Res. 66 (2006) 9646-9655
11. Elison J.R., Cobrinik D., Claros N., Abramson D.H., and Lee T.C. Small molecule inhibition of HDM2 leads to p53-mediated cell death in retinoblastoma cells. Arch. Ophthalmol. 124 (2006) 1269-1275
12. Kojima K., Konopleva M., McQueen T., O'Brien S., Plunkett W., and Andreeff M. Mdm2 inhibitor nutlin-3a induces p53-mediated apoptosis by transcription-dependent and transcription-independent mechanisms and may overcome Atm-mediated resistance to fludarabine in chronic lymphocytic leukemia. Blood 108 (2006) 993-1000
13. Coll-Mulet L., Iglesias-Serret D., Santidrian A.F., Cosialls A.M., de Frias M., Castano E., Campas C., Barragan M., de Sevilla A.F., Domingo A., Vassilev L.T., Pons G., and Gil J. MDM2 antagonists activate p53 and synergize with genotoxic drugs in B-cell chronic lymphocytic leukemia cells. Blood 107 (2006) 4109-4114
14. Stuhmer T., Chatterjee M., Hildebrandt M., Herrmann P., Gollasch H., Gerecke C., Theurich S., Cigliano L., Manz R.A., Daniel P.T., Bommert K., Vassilev L.T., and Bargou R.C. Nongenotoxic activation of the p53 pathway as a therapeutic strategy for multiple myeloma. Blood 106 (2005) 3609-3617
15. Drakos E., Thomaides A., Medeiros L.J., Li J., Leventaki V., Konopleva M., Andreeff M., and Rassidakis G.Z. Inhibition of p53-murine double minute 2 interaction by nutlin-3A stabilizes p53 and induces cell cycle arrest and apoptosis in hodgkin lymphoma. Clin. Cancer Res. 13 (2007) 3380-3387
16. Secchiero P., Barbarotto E., Tiribelli M., Zerbinati C., di Iasio M.G., Gonelli A., Cavazzini F., Campioni D., Fanin R., Cuneo A., and Zauli G. Functional integrity of the p53-mediated apoptotic pathway induced by the nongenotoxic agent nutlin-3 in B-cell chronic lymphocytic leukemia (B-CLL). Blood 107 (2006) 4122-4129
17. Turc-Carel C., Dal Cin P., Limon J., Li F., and Sandberg A.A. Translocation X;18 in synovial sarcoma. Cancer Genet. Cytogenet. 23 (1986) 93
18. Clark J., Rocques P.J., Crew A.J., Gill S., Shipley J., Chan A.M., Gusterson B.A., and Cooper C.S. Identification of novel genes, SYT and SSX, involved in the t(X;18)(p11.2;q11.2) translocation found in human synovial sarcoma. Nat. Genet. 7 (1994) 502-508
19. de Leeuw B., Balemans M., Olde Weghuis D., and Geurts van Kessel A. Identification of two alternative fusion genes, SYT-SSX1 and SYT-SSX2, in t(X;18)(p11.2;q11.2)-positive synovial sarcomas. Hum. Mol. Genet. 4 (1995) 1097-1099
20. Skytting B., Nilsson G., Brodin B., Xie Y., Lundeberg J., Uhlen M., and Larsson O. A novel fusion gene, SYT-SSX4, in synovial sarcoma. J. Natl. Cancer Inst. 91 (1999) 974-975
21. Lewis J.J., Antonescu C.R., Leung D.H., Blumberg D., Healey J.H., Woodruff J.M., and Brennan M.F. Synovial sarcoma: a multivariate analysis of prognostic factors in 112 patients with primary localized tumors of the extremity. J. Clin. Oncol. 18 (2000) 2087-2094
22. de Bruijn D.R., Allander S.V., van Dijk A.H., Willemse M.P., Thijssen J., van Groningen J.J., Meltzer P.S., and van Kessel A.G. The synovial-sarcoma-associated SS18-SSX2 fusion protein induces epigenetic gene (de)regulation. Cancer Res. 66 (2006) 9474-9482
23. Sun Y., Gao D., Liu Y., Huang J., Lessnick S., and Tanaka S. IGF2 is critical for tumorigenesis by synovial sarcoma oncoprotein SYT-SSX1. Oncogene 25 (2006) 1042-1052
24. Saito T., Nagai M., and Ladanyi M. SYT-SSX1 and SYT-SSX2 interfere with repression of E-cadherin by snail and slug: a potential mechanism for aberrant mesenchymal to epithelial transition in human synovial sarcoma. Cancer Res. 66 (2006) 6919-6927
25. Pretto D., Barco R., Rivera J., Neel N., Gustavson M.D., and Eid J.E. The synovial sarcoma translocation protein SYT-SSX2 recruits beta-catenin to the nucleus and associates with it in an active complex. Oncogene 25 (2006) 3661-3669
26. Xie Y., Skytting B., Nilsson G., Gasbarri A., Haslam K., Bartolazzi A., Brodin B., Mandahl N., and Larsson O. SYT-SSX is critical for cyclin D1 expression in synovial sarcoma cells: a gain of function of the t(X;18)(p11.2;q11.2) translocation. Cancer Res. 62 (2002) 3861-3867
27. Oda Y., Sakamoto A., Satio T., Kawauchi S., Iwamoto Y., and Tsuneyoshi M. Molecular abnormalities of p53, MDM2, and H-ras in synovial sarcoma. Mod. Pathol. 13 (2000) 994-1004
28. Schneider-Stock R., Onnasch D., Haeckel C., Mellin W., Franke D.S., and Roessner A. Prognostic significance of p53 gene mutations and p53 protein expression in synovial sarcomas. Virchows Arch. 435 (1999) 407-412
29. D'Arcy P., Maruwge W., Ryan B.A., and Brodin B. The oncoprotein SS18-SSX1 promotes p53 ubiquitination and degradation by enhancing HDM2 stability. Mol. Cancer Res. 6 (2008) 127-138
30. Kawai A., Naito N., Yoshida A., Morimoto Y., Ouchida M., Shimizu K., and Beppu Y. Establishment and characterization of a biphasic synovial sarcoma cell line, SYO-1. Cancer Lett. 204 (2004) 105-113
31. Tovar C., Rosinski J., Filipovic Z., Higgins B., Kolinsky K., Hilton H., Zhao X., Vu B.T., Qing W., Packman K., Myklebost O., Heimbrook D.C., and Vassilev L.T. Small-molecule MDM2 antagonists reveal aberrant p53 signaling in cancer: implications for therapy. Proc. Natl. Acad. Sci. USA 103 (2006) 1888-1893
32. Spurrell E.L., Fisher C., Thomas J.M., and Judson I.R. Prognostic factors in advanced synovial sarcoma: an analysis of 104 patients treated at the Royal Marsden Hospital. Ann. Oncol. 16 (2005) 437-444
33. Shieh S.Y., Ikeda M., Taya Y., and Prives C. DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91 (1997) 325-334
34. Barlev N.A., Liu L., Chehab N.H., Mansfield K., Harris K.G., Halazonetis T.D., and Berger S.L. Acetylation of p53 activates transcription through recruitment of coactivators/histone acetyltransferases. Mol. Cell 8 (2001) 1243-1254
35. Arva N.C., Gopen T.R., Talbott K.E., Campbell L.E., Chicas A., White D.E., Bond G.L., Levine A.J., and Bargonetti J. A chromatin-associated and transcriptionally inactive p53-Mdm2 complex occurs in mdm2 SNP309 homozygous cells. J. Biol. Chem. 280 (2005) 26776-26787
36. Bond G.L., Hu W., Bond E.E., Robins H., Lutzker S.G., Arva N.C., Bargonetti J., Bartel F., Taubert H., Wuerl P., Onel K., Yip L., Hwang S.-J., Strong L.C., Lozano G., and Levine A.J. A single nucleotide polymorphism in the MDM2 promoter attenuates the p53 tumor suppressor pathway and accelerates tumor formation in humans. Cell 119 (2004) 591-602