Inhibition of the p53 E3 ligase HDM-2 induces apoptosis and DNA damage - Independent p53 phosphorylation in mantle cell lymphoma

Clinical Cancer Research

Volumn 14, Issue 17, 2008, Pages 5416-5425

  Jones, Richard J ^a   Chen, Qing ^b   Voorhees, Peter ^b   Young, Ken H ^c   Bruey Sedano, Nathalie ^d   Yang, Dajun ^d   Orlowski, Robert Z ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^d Ascenta Therapeutics Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BORTEZOMIB; CASPASE 3; CASPASE 8; CASPASE 9; CYCLIN DEPENDENT KINASE INHIBITOR 1; MI 63; POLY(ADENOSINE DIPHOSPHATE RIBOSE); PROTEIN HDM 2; PROTEIN P53; PUMA PROTEIN; RAPAMYCIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; MDM2 PROTEIN, HUMAN; PROTEIN MDM2; UBIQUITIN PROTEIN LIGASE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL CYCLE ARREST; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; DNA STRAND BREAKAGE; DRUG INHIBITION; DRUG POTENTIATION; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IC 50; MANTLE CELL LYMPHOMA; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; UPREGULATION; DRUG ANTAGONISM; DRUG EFFECT; DRUG SCREENING; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

APOPTOSIS; CELL LINE, TUMOR; DNA DAMAGE; DRUG EVALUATION, PRECLINICAL; HUMANS; LYMPHOMA, MANTLE-CELL; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-MDM2; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN-PROTEIN LIGASES;

EID: 53049095963     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-08-0150     Document Type: Article

References (46)

1. Jaffe ES Harris NL, Stein H,Vardiman JW, editors. Pathology and genetics of tumours and lymphoid tissues. In: World Health Organisation classification of tumours. Lyon: WHO; 2001. p. 168-70.
2. Campo E, Raffeld M, Jaffe ES. Mantle-cell lymphoma. Semin Hematol 1999;36:115-27.
3. Swerdlow SH, Williams ME. From centrocytic to mantle cell lymphoma: a clinicopathologic and molecular review of 3 decades. Hum Pathol 2002;33:7-20.
4. Orlowski RZ, Stinchcombe TE, Mitchell BS, et al. Phase I trial of the proteasome inhibitor PS-341 in patients with refractory hematologic malignancies. J Clin Oncol 2002;20:4420-7.
5. O'Connor OA, Wright J, Moskowitz C, et al. Phase II clinical experience with the novel proteasome inhibitor bortezomib in patients with indolent non-Hodgkin's lymphoma and mantle cell lymphoma. J Clin Oncol 2005;23:676-84.
6. Goy A, Younes A, McLaughlin P, et al. Phase II study of proteasome inhibitor bortezomib in relapsed or refractory B-cell non-Hodgkin's lymphoma. J Clin Oncol 2005;23:667-75.
7. Perez-Galan P, Roue G, Villamor N, Montserrat E, Campo E, Colomer D. The proteasome inhibitor bortezomib induces apoptosis in mantle-cell lymphoma through generation of ROS and Noxa activation independent of p53 status. Blood 2006;107:257-64.
8. Haupt Y, Maya R, Kazaz A, Oren M.Mdm2 promotes the rapid degradation of p53. Nature 1997;387:296-9.
9. Momand J, Jung D, Wilczynski S, Niland J. The Mdm2 gene amplification database. Nucleic Acids Res1998;26:3453-9.
10. Finnegan MC, Goepel JR, Royds J, Hancock BW, Goyns MH. Elevated levels of Mdm-2 and p53 expression are associated with high grade non-Hodg-kin's lymphomas. Cancer Lett1994;86:215-21.
11. Lane DP. Cancer. p53, guardian of the genome. Nature1992;358:15-6.
12. Levine AJ. p53, the cellular gatekeeper for growth and division. Cell 1997;88:323-31.
13. Vassilev LT, Vu BT, Graves B, et al. In vivo activation of the p53 pathway by small-molecule antagonists of Mdm2. Science 2004;303:844-8.
14. Issaeva N, Bozko P, Enge M, et al. Small molecule Rita binds to p53, blocks p53-Hdm-2 interaction and activates p53 function in tumors. Nat Med 2004;10:1321-8.
15. Ambrosini G, Sambol EB, Carvajal D, Vassilev LT, Singer S, Schwartz GK. Mouse double minute antagonist Nutlin-3a enhances chemotherapy-induced apoptosis in cancer cells with mutant p53 by activating E2F1. Oncogene 2007;26:3473-81.
16. Logan IR, McNeill HV, Cook S, Lu X, Lunec J, Rob-son CN. Analysis of the Mdm2 antagonist Nutlin-3 in human prostate cancer cells. Prostate 2007;67:900-6.
17. LaRusch GA, Jackson MW, DunbarJD,Warren RS, Donner DB, Mayo LD. Nutlin3 blocks vascular endothelial growth factor induction by preventing the inter action between hypoxia inducible factor 1 α and Hdm2. Cancer Res 2007;67:450-4.
18. Dey A,Wong ET, Bist P,Tergaonkar V, Lane DP. Nutlin-3 inhibits the NFκB pathwayin a p53-dependent manner: implications in lung cancer therapy. Cell Cycle 2007;6:2178-85.
19. Kuhn DJ, Chen Q,Voorhees PM, et al. Potent activityof carfilzomib, a novel, irreversible inhibitor of the ubiquitin-proteasome pathway, against preclinical models of multiple myeloma. Blood 2007;110:3281-90.
20. Ookawa K, Kudo T, Aizawa S, Saito H, Tsuchida S. Transcriptional activation of the Muc2 gene byp53. J Biol Chem 2002;277:48270-5.
21. Jones RJ, Dickerson S, Bhende PM, Delecluse HJ, KenneySC. Epstein-Barr virus lytic infection induces retinoic acid-responsive genes through induction of a retinol-metabolizing enzyme, Dhrs9. J Biol Chem 2007;282:8317-24.
22. Chou TC. The median-effect principle and the combination index for quantitation of synergism and antagonism.In:ChouTC,Rideout,DC,editors. Synergism and antagonism in chemotherapy. San Diego: Academic Press;1991. p. 61-102.
23. Chou TC,Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984; 22:27-55.
24. Ding K, LuY, Nikolovska-Coleska Z, et al. Structure-based design of spiro-oxindoles as potent, specific small-molecule inhibitors of the Mdm2-53 interaction. J Med Chem 2006;49:3432-5.
25. Shangary S, Qin D, McEachern D, et al. Temporal activation of p53 by a specific Mdm2 inhibitor is selectively toxic to tumors and leads to complete tumor growth inhibition. Proc Natl Acad Sci U S A 2008;105:3933-8.
26. Komarov PG, Komarova EA, Kondratov RV, et al. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 1999;285:1733-7.
27. DrakosE,Thomaides A, Medeiros LJ, et al. 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 2007;13:3380-7.
28. Graat HC, Carette JE, Schagen FH, et al. Enhanced tumor cell kill by combined treatment with a small-molecule antagonist of mouse double minute 2 and adenoviruses encoding p53. Mol CancerTher 2007;6:1552-61.
29. Lavin MF, Gueven N. The complexityofp53 stabilization and activation. Cell Death Differ 2006;13:941-50.
30. Bewersdorf J, Bennett BT, Knight KL. H2AX chromatin structures and their response to DNA damage revealed by4Pi microscopy. Proc Natl Acad Sci U S A 2006;103:18137-42.
31. Thiriet C, Hayes JJ. Chromatin in need of a fix: phosphorylation of H2AX connects chromatin to DNA repair. Mol Cell 2005;18:617-22.
32. Hipp S, Ringshausen I, Oelsner M, Bogner C, Peschel C, Decker T. Inhibition of the mammalian target of rapamycin and the induction of cell cycle arrest in mantle cell lymphoma cells. Haematologica 2005;90:1433-4.
33. Mitsiades N, Mitsiades CS, Richardson PG, et al. The proteasome inhibitor PS-341 potentiates sensitivity of multiple myeloma cells to conventional chemotherapeutic agents: therapeutic applications. Blood 2003;101:2377-80.
34. Bertoni F, Zucca E, Cotter FE. Molecular basis of mantle cell lymphoma. Br J Haematol 2004;124:130-40.
35. Bosch F, Lopez-Guillermo A, Campo E, et al. Mantle cell lymphoma: presenting features, response to therapy, and prognostic factors. Cancer 1998;82:567-75.
36. Stuhmer T, Chatterjee M, Hildebrandt M, et al. Nongenotoxic activation of the p53 pathway as a therapeutic strategy for multiple myeloma. Blood 2005;106:3609-17.
37. Secchiero P, Barbarotto E,Tiribelli M, et al. Functional integrity of the p53-mediated apoptotic pathway induced by the nongenotoxic agent Nutlin-3 in B-cell chronic lymphocytic leukemia (B-CLL). Blood 2006;107:4122-9.
38. ThompsonT,Tovar C,Yang H, et al. Phosphorylation of p53 on key serines is dispensable for transcriptional activation and apoptosis. J Biol Chem 2004;279:53015-22.
39. Efeyan A, Ortega-Molina A,Velasco-Miguel S, Herranz D,Vassilev LT, Serrano M. Induction of p53-de-pendent senescence by the Mdm2 antagonist Nutlin-3a in mouse cells of fibroblast origin. Cancer Res 2007;67:7350-7.
40. Jiang M, Pabla N, Murphy RF, et al. Nutlin-3 protects kidney cells during cisplatin therapy by suppressing Bax/Bak activation. J Biol Chem 2007;282:2636-45.
41. Hupp TR, Meek DW, Midgley CA, Lane DP. Regulation of the specific DNA binding function of p53. Cell 1992;71:875-86.
42. Yap DB, Hsieh JK, Zhong S, et al. Ser392 phosphorylation regulates the oncogenic function of mutant p53. Cancer Res 2004;64:4749-54.
43. Lau LM, Nugent JK, Zhao X, Irwin MS. Hdm2 antagonist Nutlin-3 disrupts p73-2 binding and enhances p73 function. Oncogene 2007;27:997-1003.
44. Lin J, Chen J, Elenbaas B, Levine AJ. Several hydrophobic amino acids in the p53 amino-terminal domain are required for transcriptional activation, binding to Mdm-2 and the adenovirus 5 E1B 55-kD protein. Genes Dev1994;8:1235-46.
45. Picksley SM,Vojtesek B, Sparks A, Lane DP. Immunochemical analysis of the interaction of p53 with Mdm2; fine mapping of the mdm-2 binding site on p53 using synthetic peptides. Oncogene 1994;9:2523-9.
46. Carvajal D, Tovar C, Yang H, Vu BT, Heimbrook DC, Vassilev LT. Activation of p53 byMdm2 antagonists can protect proliferating cells from mitotic inhibitors. Cancer Res 2005;65:1918-24.