p53-dependent regulation of Mcl-1 contributes to synergistic cell death by ionizing radiation and the Bcl-2/Bcl-XL inhibitor ABT-737

Apoptosis

Volumn 17, Issue 2, 2012, Pages 187-199

  Tagscherer, Katrin E ^a   Fassl, Anne ^a   Sinkovic, Tabea ^a,b   Combs, Stephanie E ^b   Roth, Wilfried ^a,b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

ABT 737; Apoptosis; Bcl 2 inhibitor; Ionizing radiation; Mcl 1; p53

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MCL 1; PROTEIN P21; PROTEIN P53;

APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CONTROLLED STUDY; DRUG EFFECT; GLIOBLASTOMA; HUMAN; HUMAN CELL; IONIZING RADIATION; PRIORITY JOURNAL; PROTEIN FUNCTION;

APOPTOSIS; BCL-X PROTEIN; BIPHENYL COMPOUNDS; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P21; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; NITROPHENOLS; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-BCL-2; RADIATION, IONIZING; RNA, SMALL INTERFERING; SULFONAMIDES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84862500662     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-011-0664-3     Document Type: Article

References (57)

1. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, Belli BA et al (2005) An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435(7042):677-681. doi:10.1038/nature03579 (Pubitemid 40825512)
2. Del Gaizo Moore V, Brown JR, Certo M, Love TM, Novina CD, Letai A (2007) Chronic lymphocytic leukemia requires BCL2 to sequester prodeath BIM, explaining sensitivity to BCL2 antagonist ABT-737. J Clin Invest 117(1):112-121 (Pubitemid 46048458)
3. Okumura K, Huang S, Sinicrope FA (2008) Induction of Noxa sensitizes human colorectal cancer cells expressing Mcl-1 to the small-molecule Bcl-2/Bcl-xL inhibitor, ABT-737. Clin Cancer Res 14(24):8132-8142. doi:10.1158/1078-0432.CCR-08-1665
4. Vogler M, Dinsdale D, Dyer MJ, Cohen GM (2009) Bcl-2 inhibitors: small molecules with a big impact on cancer therapy. Cell Death Differ 16(3):360-367. doi:10.1038/cdd.2008.137
5. Labi V, Grespi F, Baumgartner F, Villunger A (2008) Targeting the Bcl-2-regulated apoptosis pathway by BH3 mimetics: a breakthrough in anticancer therapy? Cell Death Differ 15(6):977-987. doi:10.1038/cdd.2008.37 (Pubitemid 351712602)
6. Tse C, Shoemaker AR, Adickes J, Anderson MG, Chen J, Jin S et al (2008) ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor. Cancer Res 68(9):3421-3428. doi:10.1158/0008-5472.CAN-07-5836
7. Park CM, Bruncko M, Adickes J, Bauch J, Ding H, Kunzer A et al (2008) Discovery of an orally bioavailable small molecule inhibitor of prosurvival B-cell lymphoma 2 proteins. J Med Chem 51(21):6902-6915. doi:10.1021/jm800669s
8. Tagscherer KE, Fassl A, Campos B, Farhadi M, Kraemer A, Bock BC et al (2008) Apoptosis-based treatment of glioblastomas with ABT-737, a novel small molecule inhibitor of Bcl-2 family proteins. Oncogene 27(52):6646-6656. doi:10.1038/onc.2008.259
9. Chen S, Dai Y, Pei XY, Grant S (2009) Bim upregulation by histone deacetylase inhibitors mediates interactions with the Bcl-2 antagonist ABT-737: evidence for distinct roles for Bcl-2, Bcl-xL, and Mcl-1. Mol Cell Biol 29(23):6149-6169. doi:10.1128/MCB.01481-08
10. Mason KD, Khaw SL, Rayeroux KC, Chew E, Lee EF, Fairlie WD et al (2009) The BH3 mimetic compound, ABT-737, synergizes with a range of cytotoxic chemotherapy agents in chronic lymphocytic leukemia. Leukemia 23(11):2034-2041. doi:10.1038/leu.2009.151
11. Zall H, Weber A, Besch R, Zantl N, Hacker G (2010) Chemotherapeutic drugs sensitize human renal cell carcinoma cells to ABT-737 by a mechanism involving the Noxa-dependent inactivation of Mcl-1 or A1. Mol Cancer 9:164. doi:10.1186/1476-4598-9-164
12. Cragg MS, Harris C, Strasser A, Scott CL (2009) Unleashing the power of inhibitors of oncogenic kinases through BH3 mimetics. Nat Rev Cancer 9(5):321-326. doi:10.1038/nrc2615
13. Morales AA, Gutman D, Lee KP, Boise LH (2008) BH3-only proteins Noxa, Bmf, and Bim are necessary for arsenic trioxide-induced cell death in myeloma. Blood 111(10):5152-5162. doi:10.1182/blood-2007-10-116889
14. Miller LA, Goldstein NB, Johannes WU, Walton CH, Fujita M, Norris DA et al (2009) BH3 mimetic ABT-737 and a proteasome inhibitor synergistically kill melanomas through Noxa-dependent apoptosis. J Invest Dermatol 129(4):964-971. doi:10.1038/jid.2008.327
15. Yecies D, Carlson NE, Deng J, Letai A (2010) Acquired resistance to ABT-737 in lymphoma cells that up-regulate MCL-1 and BFL-1. Blood 115(16):3304-3313. doi:10.1182/blood-2009-07-233304
16. Kang MH, Wan Z, Kang YH, Sposto R, Reynolds CP (2008) Mechanism of synergy of N-(4-hydroxyphenyl)retinamide and ABT-737 in acute lymphoblastic leukemia cell lines: Mcl-1 inactivation. J Natl Cancer Inst 100(8):580-595
17. Zhang W, Konopleva M, Ruvolo VR, McQueen T, Evans RL, Bornmann WG et al (2008) Sorafenib induces apoptosis of AML cells via Bim-mediated activation of the intrinsic apoptotic pathway. Leukemia 22(4):808-818. doi:10.1038/sj.leu. 2405098 (Pubitemid 351552630)
18. Adams JM, Cory S (2007) Bcl-2-regulated apoptosis: mechanism and therapeutic potential. Curr Opin Immunol 19(5):488-496. doi:10.1016/j.coi.2007. 05.004 (Pubitemid 47487452)
19. Kojima K, Konopleva M, Samudio IJ, Schober WD, Bornmann WG, Andreeff M (2006) Concomitant inhibition of MDM2 and Bcl-2 protein function synergistically induce mitochondrial apoptosis in AML. Cell Cycle 5(23):2778-2786 (Pubitemid 44901740)
20. Schmitt M, Pawlita M (2009) High-throughput detection and multiplex identification of cell contaminations. Nucleic Acids Res 37(18):e119. doi:10.1093/nar/gkp581
21. Van Meir EG, Kikuchi T, Tada M, Li H, Diserens AC, Wojcik BE et al (1994) Analysis of the p53 gene and its expression in human glioblastoma cells. Cancer Res 54(3):649-652 (Pubitemid 24068319)
22. Bivik C, Ollinger K (2008) JNK mediates UVB-induced apoptosis upstream lysosomal membrane permeabilization and Bcl-2 family proteins. Apoptosis 13(9):1111-1120. doi:10.1007/s10495-008-0240-7
23. Nijhawan D, Fang M, Traer E, Zhong Q, Gao W, Du F et al (2003) Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation. Genes Dev 17(12):1475-1486. doi:10.1101/gad.1093903 (Pubitemid 36734705)
24. Kubota Y, Kinoshita K, Suetomi K, Fujimori A, Takahashi S (2007) Mcl-1 depletion in apoptosis elicited by ionizing radiation in peritoneal resident macrophages of C3H mice. J Immunol 178(5):2923-2931 (Pubitemid 46333171)
25. Tichy A, Zaskodova D, Pejchal J, Rezacova M, Osterreicher J, Vavrova J et al (2008) Gamma irradiation of human leukaemic cells HL-60 and MOLT-4 induces decrease in Mcl-1 and Bid, release of cytochrome c, and activation of caspase-8 and caspase-9. Int J Radiat Biol 84(6):523-530. doi:10.1080/09553000802078404 (Pubitemid 351878836)
26. Willis SN, Adams JM (2005) Life in the balance: how BH3-only proteins induce apoptosis. Curr Opin Cell Biol 17(6):617-625. doi:10.1016/j.ceb.2005.10. 001 (Pubitemid 41540411)
27. Vesely J, Havlicek L, Strnad M, Blow JJ, Donella-Deana A, Pinna L et al (1994) Inhibition of cyclin-dependent kinases by purine analogues. Eur J Biochem 224(2):771-786 (Pubitemid 24282865)
28. Chaturvedi V, Sitailo LA, Qin JZ, Bodner B, Denning MF, Curry J et al (2005) Knockdown of p53 levels in human keratinocytes accelerates Mcl-1 and Bcl-x(L) reduction thereby enhancing UV-light induced apoptosis. Oncogene 24(34):5299-5312. doi:10.1038/sj.onc.1208650 (Pubitemid 43080100)
29. Batista LF, Roos WP, Christmann M, Menck CF, Kaina B (2007) Differential sensitivity of malignant glioma cells to methylating and chloroethylating anticancer drugs: p53 determines the switch by regulating xpc, ddb2, and DNA double-strand breaks. Cancer Res 67(24):11886-11895. doi:10.1158/0008-5472.CAN- 07-2964
30. Biroccio A, Bufalo DD, Ricca A, D'Angelo C, D'Orazi G, Sacchi A et al (1999) Increase of BCNU sensitivity by wt-p53 gene therapy in glioblastoma lines depends on the administration schedule. Gene Ther 6(6):1064-1072. doi:10.1038/sj.gt.3300935 (Pubitemid 29295212)
31. Broaddus WC, Liu Y, Steele LL, Gillies GT, Lin PS, Loudon WG et al (1999) Enhanced radiosensitivity of malignant glioma cells after adenoviral p53 transduction. J Neurosurg 91(6):997-1004. doi:10.3171/jns.1999.91.6.0997
32. Wade M, Rodewald LW, Espinosa JM, Wahl GM (2008) BH3 activation blocks Hdmx suppression of apoptosis and cooperates with Nutlin to induce cell death. Cell Cycle 7(13):1973-1982 (Pubitemid 352030342)
33. Reiners JJ Jr, Kessel D (2005) Susceptibility of myelomonocytic leukemia U937 cells to the induction of apoptosis by the non-peptidic Bcl-2 ligand HA14-1 is cell cycle phase-dependent. Cancer Lett 221(2):153-163. doi:10.1016/j. canlet.2004.09.012
34. Choudhuri T, Pal S, Das T, Sa G (2005) Curcumin selectively induces apoptosis in deregulated cyclin D1-expressed cells at G2 phase of cell cycle in a p53-dependent manner. J Biol Chem 280(20):20059-20068. doi:10.1074/jbc. M410670200 (Pubitemid 41379535)
35. Shu CH, Yang WK, Shih YL, Kuo ML, Huang TS (1997) Cell cycle G2/M arrest and activation of cyclin-dependent kinases associated with low-dose paclitaxel-induced sub-G1 apoptosis. Apoptosis 2(5):463-470 (Pubitemid 127508257)
36. Carter BZ, Mak DH, Woessner R, Gross S, Schober WD, Estrov Z et al (2009) Inhibition of KSP by ARRY-520 induces cell cycle block and cell death via the mitochondrial pathway in AML cells. Leukemia 23(10):1755-1762. doi:10.1038/leu.2009.101
37. Blagosklonny MV (2007) Mitotic arrest and cell fate: why and how mitotic inhibition of transcription drives mutually exclusive events. Cell Cycle 6(1):70-74
38. Singh R, George J, Shukla Y (2010) Role of senescence and mitotic catastrophe in cancer therapy. Cell Div 5:4. doi:10.1186/1747-1028-5-4
39. Quick QA, Gewirtz DA (2006) An accelerated senescence response to radiation in wild-type p53 glioblastoma multiforme cells. J Neurosurg 105(1):111-118. doi:10.3171/jns.2006.105.1.111 (Pubitemid 43979105)
40. Pollack IF, Hamilton RL, Finkelstein SD, Campbell JW, Martinez AJ, Sherwin RN et al (1997) The relationship between TP53 mutations and overexpression of p53 and prognosis in malignant gliomas of childhood. Cancer Res 57(2):304-309 (Pubitemid 27036787)
41. Rich JN, Hans C, Jones B, Iversen ES, McLendon RE, Rasheed BK et al (2005) Gene expression profiling and genetic markers in glioblastoma survival. Cancer Res 65(10):4051-4058. doi:10.1158/0008-5472.CAN-04-3936 (Pubitemid 40775641)
42. Weller M, Felsberg J, Hartmann C, Berger H, Steinbach JP, Schramm J et al (2009) Molecular predictors of progression-free and overall survival in patients with newly diagnosed glioblastoma: a prospective translational study of the German Glioma Network. J Clin Oncol 27(34):5743-5750. doi:10.1200/JCO.2009. 23.0805
43. Wang JM, Chao JR, Chen W, Kuo ML, Yen JJ, Yang-Yen HF (1999) The antiapoptotic gene mcl-1 is up-regulated by the phosphatidylinositol 3-kinase/Akt signaling pathway through a transcription factor complex containing CREB. Mol Cell Biol 19(9):6195-6206 (Pubitemid 29399324)
44. Giebler HA, Lemasson I, Nyborg JK (2000) p53 recruitment of CREB binding protein mediated through phosphorylated CREB: a novel pathway of tumor suppressor regulation. Mol Cell Biol 20(13):4849-4858 (Pubitemid 30396131)
45. Pietrzak M, Puzianowska-Kuznicka M (2008) p53-dependent repression of the human MCL-1 gene encoding an anti-apoptotic member of the BCL-2 family: the role of Sp1 and of basic transcription factor binding sites in the MCL-1 promoter. Biol Chem 389(4):383-393. doi:10.1515/BC.2008.039 (Pubitemid 351773909)
46. Thomas LW, Lam C, Edwards SW (2010) Mcl-1; the molecular regulation of protein function. FEBS Lett 584(14):2981-2989. doi:10.1016/j.febslet.2010.05.061
47. Akgul C (2009) Mcl-1 is a potential therapeutic target in multiple types of cancer. Cell Mol Life Sci 66(8):1326-1336. doi:10.1007/s00018-008-8637-6
48. Lin J, Tang H, Jin X, Jia G, Hsieh JT (2002) p53 regulates Stat3 phosphorylation and DNA binding activity in human prostate cancer cells expressing constitutively active Stat3. Oncogene 21(19):3082-3088. doi:10.1038/sj.onc.1205426 (Pubitemid 34522909)
49. Fritsche M, Mundt M, Merkle C, Jahne R, Groner B (1998) p53 suppresses cytokine induced, Stat5 mediated activation of transcription. Mol Cell Endocrinol 143(1-2):143-154 (Pubitemid 28458751)
50. Sermeus A, Michiels C (2011) Reciprocal influence of the p53 and the hypoxic pathways. Cell Death Dis 2:e164. doi:10.1038/cddis.2011.48
51. Shmueli A, Oren M (2005) Life, death, and ubiquitin: taming the mule. Cell 121(7):963-965. doi:10.1016/j.cell.2005.06.018 (Pubitemid 40884386)
52. Ploner C, Kofler R, Villunger A (2008) Noxa: at the tip of the balance between life and death. Oncogene 27(Suppl 1):S84-S92. doi:10.1038/onc.2009.46
53. Racay P, Hatok J, Hudecek J, Chudej J, Jurecekova J, Dobrota D (2008) Transcription of genes of p53-dependent apoptosis in acute leukaemia. Int J Mol Med 22(6):833-839
54. Hauck P, Chao BH, Litz J, Krystal GW (2009) Alterations in the Noxa/Mcl-1 axis determine sensitivity of small cell lung cancer to the BH3 mimetic ABT-737. Mol Cancer Ther 8(4):883-892. doi:10.1158/1535-7163.MCT-08-1118
55. Chen S, Dai Y, Harada H, Dent P, Grant S (2007) Mcl-1 downregulation potentiates ABT-737 lethality by cooperatively inducing Bak activation and Bax translocation. Cancer Res 67(2):782-791 (Pubitemid 46192219)
56. High LM, Szymanska B, Wilczynska-Kalak U, Barber N, O'Brien R, Khaw SL et al (2010) The Bcl-2 homology domain 3 mimetic ABT-737 targets the apoptotic machinery in acute lymphoblastic leukemia resulting in synergistic in vitro and in vivo interactions with established drugs. Mol Pharmacol 77(3):483-494. doi:10.1124/mol.109.060780
57. Lin X, Morgan-Lappe S, Huang X, Li L, Zakula DM, Vernetti LA et al (2007) 'Seed' analysis of off-target siRNAs reveals an essential role of Mcl-1 in resistance to the small-molecule Bcl-2/Bcl-XL inhibitor ABT-737. Oncogene 26(27):3972-3979 (Pubitemid 46884293)