Inhibition of c-Jun-N-terminal-kinase sensitizes tumor cells to CD95-induced apoptosis and induces G2/M cell cycle arrest

Cancer Research

Volumn 65, Issue 15, 2005, Pages 6780-6788

  Kuntzen, Christian ^a,b   Sonuc, Nilüfer ^a   De Toni, Enrico N ^a   Opelz, Christine ^a   Mucha, Simon R ^a   Gerbes, Alexander L ^a   Eichhorst, Sören T ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CASPASE 3; CASPASE 8; CYCLIN DEPENDENT KINASE INHIBITOR 1; DACTINOMYCIN; FAS ANTIGEN; MESYLIC ACID METHYL ESTER; PROTEIN P21; PROTEIN P53; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; TUMOR NECROSIS FACTOR;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CELL CYCLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TUMOR CELL; UPREGULATION;

ANTHRACENES; ANTIGENS, CD95; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CASPASE 3; CASPASE 8; CASPASES; CELL CYCLE PROTEINS; CELL DIVISION; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P21; ENZYME ACTIVATION; G2 PHASE; HUMANS; JURKAT CELLS; LIVER NEOPLASMS; MITOGEN-ACTIVATED PROTEIN KINASE 8; MITOGEN-ACTIVATED PROTEIN KINASE 9; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-JUN; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 23044453047     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-04-2618     Document Type: Article

References (48)

1. Eichhorst ST, Krueger A, Muerkoster S, et al. Suramin inhibits death receptor-induced apoptosis in vitro and fulminant apoptotic liver damage in mice. Nat Med 2004;10:602-9.
2. O'Connell J, Bennett MW, Nally K, Houston A, O'Sullivan GC, Shanahan F. Altered mechanisms of apoptosis in colon cancer: Fas resistance and counterattack in the tumor-immune conflict. Ann N Y Acad Sci 2000;910:178-92.
3. Owen-Schaub LB, Zhang W, Cusack JC, et al. Wild-type human p53 and a temperature-sensitive mutant induce Fas/APO-1 expression. Cancer Lett 1995;94:1-8.
4. Okano H, Shiraki K, Inoue H, et al. Cellular FLICE/caspase-8-inhibitory protein as a principal regulator of cell death and survival in human hepatocellular carcinoma. Lab Invest 2003;83:1033-43.
5. Ito Y, Monden M, Takeda T, et al. The status of Fas and Fas ligand expression can predict recurrence of hepatocellular carcinoma. Br J Cancer 2000;82: 1211-7.
6. Krammer PH. CD95's deadly mission in the immune system. Nature 2000;407:789-95.
7. Peter ME, Scaffidi C, Medema JP, Kischkel F, Krammer PH. The death receptors. Results Probl Cell Differ 1999;23:25-63.
8. Scaffidi C, Fulda S, Srinivasan A, et al. Two CD95 (APO-1/Fas) signaling pathways. EMBO J 1998;17: 1675-87.
9. Eferl R, Sibilia M, Hilberg F, et al. Functions of c-Jun in liver and heart development J Cell Biol 1999;145: 1049-61.
10. Eichhorst ST, Muller M, Li-Weber M, Schulze-Bergkamen H, Angel P, Krammer PH. A Novel AP-1 element in the CD95 ligand promoter is required for induction of apoptosis in hepatocellular carcinoma cells upon treatment with anticancer drugs. Mol Cell Biol 2000;20:7826-37.
11. Kondoh N, Wakatsuki T, Hada A, et al. Genetic and epigenetic events in human hepatocarcinogenesis. Int J Oncol 2001;18:1271-8.
12. Schmidt CM, McKillop IH, Cahili PA, Sitzmann JV. The role of cAMP-MAPK signalling in the regulation of human hepatocellular carcinoma growth in vitro. Eur J Gastroenterol Hepatol 1999;11:1393-9.
13. Schmidt CM, McKillop IH, Cahill PA, Sitzmann JV. Increased MAPK expression and activity in primary human hepatocellular carcinoma. Biochem Biophys Res Commun 1997;236:54-8.
14. Huynh HT, Nguyen TT, Chow PK, Tan PH, Soo KC, Tran E. Over-expression of MEK-MAPK in hepatocellular carcinoma: its role in tumor progression and apoptosis. BMC Gastroenterol 2003;3:19.
15. Eferl R, Ricci R, Kenner L, et al. Liver tumor development. c-Jun antagonizes the proapoptotic activity of p53. Cell 2003;112:181-92.
16. Nicoletti I, Migliorati G, Pagliacci MC, Grignani F, Riccardi C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J Immunol Methods 1991;139: 271-9.
17. Finzer P, Kuntzen C, Soto U, zur Hausen H, Rosl F. Inhibitors of histone deacetylase arrest cell cycle and induce apoptosis in cervical carcinoma cells circumventing human papillomavirus oncogene expression. Oncogene 2001;20:4768-76.
18. Krueger A, Schmitz I, Baumann S, Krammer PH, Kirchhoff S. Cellular FLICE-inhibitory protein splice variants inhibit different steps of caspase-8 activation at the CD95 death-inducing signaling complex. J Biol Chem 2001;276:20633-40.
19. Mak TW, Yeh WC. Signaling for survival and apoptosis in the immune system. Arthritis Res 2002; 4:S243-52.
20. Leppa S, Bohmann D. Diverse functions of JNK signaling and c-Jun in stress response and apoptosis. Oncogene 1999;18:6158-62.
21. Potapova O, Gorospe M, Dougherty RH, Dean NM, Gaarde WA, Holbrook NJ. Inhibition of c-Jun N-terminal kinase 2 expression suppresses growth and induces apoptosis of human tumor cells in a p53-dependent manner. Mol Cell Biol 2000;20:1713-22.
22. Kolbus A, Herr I, Schreiber M, Debatin KM, Wagner EF, Angel P. c-Jun dependent CD95-L expression is a rate-limiting step in the induction of apoptosis by alkylating agents. Mol Cell Biol 2000;20: 575-82.
23. Angel P, Hattori K, Smeal T, Karin M. The jun protooncogene is positively autoregulated by its product, Jun/AP-1. Cell 1988;55:875-85.
24. Muller M, Strand S, Hug H, et al. Drug-induced apoptosis in hepatoma cells is mediated by the CD95 (APO-1/Fas) receptor/ligand system and involves activation of wild-type p53. J Clin Invest 1997;99: 403-13.
25. Polyak K, Waldman T, He TC, Kinzler KW, Vogelstein B. Genetic determinants of p53-induced apoptosis and growth arrest. Genes Dev 1996;10:1945-52.
26. Suzuki A, Tsutomi Y, Yamamoto N, Shibutani T, Akahane K. Mitochondrial regulation of cell death: mitochondria are essential for procaspase 3-p21 complex formation to resist Fas-mediated cell death. Mol Cell Biol 1999;19:3842-7.
27. Lamb JA, Ventura JJ, Hess P, Flavell RA, Davis RJ. JunD mediates survival signaling by the JNK signal transduction pathway. Mol Cell 2003;11:1479-89.
28. Weitzman JB, Fiette L, Matsuo K, Yaniv M. JunD protects cells from p53-dependent senescence and apoptosis. Mol Cell 2000;6:1109-19.
29. Davis RJ. Signal transduction by the JNK group of MAP kinases. Cell 2000;103:239-52.
30. 2-terminal kinase activation, and defects in AP-1 transcriptional activity. Proc Natl Acad Sci U S A 1997;94:3004-9.
31. Bennett BL, Sasaki DT, Murray BW, et al. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci U S A 2001;98:13681-6.
32. Liu ZG, Hsu H, Goeddel DV, Karin M. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-κB activation prevents cell death. Cell 1996;87:565-76.
33. Natoli G, Costanzo A, Ianni A, et al. Activation of SAPK/JNK by TNF receptor 1 through a noncytotoxic TRAF2-dependent pathway. Science 1997;275:200-3.
34. Tang G, Minemoto Y, Dibling B, et al. Inhibition of JNK activation through NF-κB target genes. Nature 2001;414:313-7.
35. De Smaele E, Zazzeroni F, Papa S, et al. Induction of gadd45β by NF-κB down-regulates pro-apoptotic JNK signalling. Nature 2001;414:308-13.
36. Deng Y, Ren X, Yang L, Lin Y, Wu X. A JNK-dependent pathway is required for TNFα-induced apoptosis. Cell 2003;115:61-70.
37. Brantley-Finley C, Lyle CS, Du L, et al. The JNK, ERK and p53 pathways play distinct roles in apoptosis mediated by the antitumor agents vinblastinc, doxorubicin, and etoposide. Biochem Pharmacol 2003;66: 459-69.
38. Mingo-Sion AM, Marietta PM, Koller E, Wolf DM, Van Den Berg CL. Inhibition of JNK reduces G2/M transit independent of p53, leading to endoreduplication, decreased proliferation, and apoptosis in breast cancer cells. Oncogene 2004;23:596-604.
39. Hu R, Kim BR, Chen C, Hebbar V, Kong AN. The roles of JNK and apoptotic signaling pathways in PEITC-mediated responses in human HT-29 colon adenocarcinoma cells. Carcinogenesis 2003;24:1361-7.
40. Bae MA, Song BJ. Critical role of c-jun N-terminal protein kinase activation in troglitazone-induced apoptosis of human HepG2 hepatoma cells. Mol Pharmacol 2003;63:401-8.
41. Chauhan D, Li G, Hideshima T, et al. JNK-dependent release of mitochondrial protein, Smac, during apoptosis in multiple myeloma (MM) cells. J Biol Chem 2003; 278:17593-6.
42. Vivo C, Liu W, Broaddus VC. c-Jun N-terminal kinase contributes to apoptotic synergy induced by tumor necrosis factor-related apoptosis-inducing ligand plus DNA damage in chemoresistant, p53 inactive mesothelioma cells. J Biol Chem 2003;278: 25461-7.
43. Ivanov VN, Krasilnikov M, Ronai Z. Regulation of Fas expression by STAT3 and c-Jun is mediated by phosphatidylinositol 3-kinase-AKT signaling. J Biol Chem 2002;277:4932-44.
44. Schreiber M, Kolbus A, Piu F, et al. Control of cell cycle progression by c-Jun is p53 dependent. Genes Dev 1999;13:607-19.
45. Suzuki A, Tsutomi Y, Miura M, Akahane K. Caspase 3 inactivation to suppress Fas-mediated apoptosis: identification of binding domain with p21 and ILP and inactivation machinery by p21. Oncogene 1999;18: 1239-44.
46. Holmstrom TH, Schmitz I, Soderstrom TS, et al. MAPK/ERK signaling in activated T cells inhibits CD95/Fas-mediated apoptosis downstream of DISC assembly. EMBO J 2000;19:5418-28.
47. Taylor WR, Stark GR. Regulation of the G2/M transition by p53. Oncogene 2001;20:1803-15.
48. Higaki K, Yano H, Kojiro M. Fas antigen expression and its relationship with apoptosis in human hepatocellular carcinoma and noncancerous tissues. Am J Pathol 1996;149:429-37.