Etoposide upregulates Bax-enhancing tumour necrosis factor-related apoptosis inducing ligand-mediated apoptosis in the human hepatocellular carcinoma cell line QGY-7703

European Journal of Biochemistry

Volumn 270, Issue 13, 2003, Pages 2721-2731

  Miao, Lin ^a   Yi, Peng ^a   Wang, Yi ^a   Wu, Mian ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

Bax; Death receptor; Mitochondrial pathway; p53; tBid

Indexed keywords

BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE 3; CASPASE 7; CASPASE 8; CASPASE 9; CYTOCHROME C; DEATH RECEPTOR 4; DEATH RECEPTOR 5; DECOY RECEPTOR 2; ETOPOSIDE; MESSENGER RNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN; PROTEIN BAX; RECEPTOR PROTEIN; RECOMBINANT PROTEIN; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; TRAIL RECEPTOR; TRUNCATED BID PROTEIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER CELL DESTRUCTION; CELL STRAIN QGY 7703; CONTROLLED STUDY; CYTOTOXICITY; DRUG MECHANISM; DRUG MIXTURE; DRUG POTENTIATION; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CARCINOMA; CARRIER PROTEINS; CASPASES; CELL SURVIVAL; CYTOCHROME C GROUP; ETOPOSIDE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER NEOPLASMS; MEMBRANE GLYCOPROTEINS; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; RECEPTORS, TUMOR NECROSIS FACTOR; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR CELLS, CULTURED; TUMOR NECROSIS FACTOR-ALPHA; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0038045649     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2003.03639.x     Document Type: Article

References (56)

1. Pitti, R.M., Marsters, S.A., Ruppert, S., Donahue, C.J., Moore, A. & Ashkenazi, A. (1996) Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J. Biol. Chem. 271, 12687-12690.
2. Wiley, S.R., Schooley, K., Smolak, P.J., Din, W.S., Huang, C.-P., Nicholl, J.K., Sutherland, G.R., Smith, T.D., Rauch, C., Smith, C.A. & Goodwin, R.G. (1995) Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 3, 673-682.
3. French, L.E. & Tschopp, J. (1999) The TRAIL to selective tumor death. Nat. Med. 5, 146-147.
4. Walczak, H., Miller, R.E., Ariail, K., Gliniak, B., Griffith, T.S., Kubin, M., Chin, W., Jones, J., Woodward, A., Le, T., Smith, C., Smolak, P., Goodwin, R.G., Rauch, C.T., Schuh, J.C. & Lynch, D.H. (1999) Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat. Med. 5, 157-163.
5. Ashkenazi, A., Pai, R.C., Fong, S., Leung, S., Lawrence, D.A., Marsters, S.A., Blackie, C., Chang, L., McMurtrey, A.E., Hebert, A., DeForge, L., Koumenis, I.L., Lewis, D., Harris, L., Bussiere, J., Koeppen, H., Shahrokh, Z. & Schwall, R.H. (1999) Safety and antitumor activity of recombinant soluble Apo2 ligand. J. Clin. Invest. 104, 155-162.
6. Pan, G., O'Rourke, K., Chinnaiyan, A.M., Gentz, R., Ebner, R., Ni, J. & Dixit, V.M. (1997) The receptor for the cytotoxic ligand TRAIL. Science 276, 111-113.
7. Pan, G., Ni, J., Wei, Y.-F., Yu, G., Gentz, R. & Dixit, V.M. (1997) An antagonist decoy receptor and a death domain-containing receptor for TRAIL. Science 277, 815-818.
8. Walczak, H., Degli-Esposti, M.A., Johnson, R.S., Smolak, P.J., Waugh, J.Y., Boiani, N., Timour, M.S., Gerhart, M.J., Schooley, K.A., Smith, C.A., Goodwin, R.G. & Rauch, C.T. (1997) TRAIL-R2: a novel apoptosis-mediating receptor for TRAIL. EMBO J. 16, 5386-5397.
9. Degli-Esposti, M.A., Smolak, P.J., Walczak, H., Waugh, J., Huang, C.-P., DuBose, R.F., Goodwin, R.G. & Smith, C.A. (1997) Cloning and characterization of TRAIL-R3, a novel member of the emerging TRAIL receptor farmly. J. Exp. Med. 186, 1165-1170.
10. Sheridan, J.P., Marsters, S.A., Pitti, R.M., Gurney, A., Skubatch, M., Baldwin, D., Ramakrishnan, L., Gray, C.L., Baker, K., Wood, W.I., Goddard, A.D., Godowski, P. & Ashkenazi, A. (1997) Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 277, 818-821.
11. Schneider, P., Bodmer, J.L., Thome, M., Hofmann, K., Holler, N. & Tschopp, J. (1997) Characterization of two receptors for TRAIL. FEBS Lett. 416, 329-334.
12. Pan, G., Ni, J., Yu, G., Wei, Y.F. & Dixit, V.M. (1998) TRUNDD, a new member of the TRAIL receptor family that antagonizes TRAIL signalling. FEBS Lett. 424, 41-45.
13. Marsters, S.A., Sheridan, J.P., Pitti, R.M., Huang, A., Skubatch, M., Baldwin, D., Yuan, J., Gurney, A., Goddard, A.D., Godowski, P. & Ashkenazi, A. (1997) A novel receptor for Apo2L/TRAIL contains a truncated death domain. Curr. Biol. 7, 1003-1006.
14. Ashkenazi, A. & Dixit, M.V. (1998) Death receptors: signaling and modulation. Science 281, 1305-1308.
15. Schneider, P., Thome, M., Burns, K., Bodmer, J-L., Hofmann, K., Kataoka, T., Holler, N. & Tschopp, J. (1997) TRAIL receptors 1 (DR4) and 2 (DR5) signal FADD-dependent apoptosis and activate NF-B. Immunity 7, 831-836.
16. Tadaaki, M. & John, C.R. (2001) A GTP-binding adapter protein couples TRAIL receptors to apoptosis-inducing proteins. Nature 2, 493-500.
17. Sheikh, M.S. & Albert, J.F. (2000) Role of p53 family members in apoptosis. J. Cell. Physiol. 182, 171-181.
18. Timothy, F.B. & Wafik, S. (1999) The p53 pathway and apoptosis. J. Cell. Physiol. 181, 231-239.
19. Alain, G.Z., Karin, R., Jennifer, B., Martin, W. & Martin, H. (2000) New insights into p53 regulation and gene therapy for cancer. Biochem. Pharmacol. 60, 1153-1163.
20. Nagane, M., Pan, G., Weddle, J.J., Dixit, V.M., Cavenee, W.K. & Huang, H.J. (2000) Increased death receptor 5 expression by chemotherapeutic agents in human gliomas causes synergistic cytotoxicity with tumor necrosis factor-related apoptosis-inducing ligand in vitro and in vivo. Cancer Res. 15, 847-853.
21. Gibson, S.B., Oyer, R., Spalding, A.C., Anderson, S.M. & Johnson, G.L. (2000) Increased expression of death receptors 4 and 5 synergizes the apoptosis response to combined treatment with etoposide and TRAIL. Mol. Cell. Biol. 20, 205-212.
22. Raymond, D.M. & Wafik, S. (2000) p53-independent upregulation of KILLER/DR5 TRAIL receptor expression by glucocorticoids and interferon-γ. Exp. Cell Res. 262, 154-169.
23. Nimmanapalli, R., Perkins, C.L., Orlando, M., O'Bryan, E., Nguyen, D. & Bhalla, K.N. (2001) Pretreatment with paclitaxel enhances Apo-2 ligand/tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis of prostate cancer cells by inducing death receptors 4 and 5 protein levels. Cancer Res. 61, 759-763.
24. LeBlanc, H., Lawrence, D., Varfolomeev, E., Totpal, K., Morlan, J., Schow, P., Fong, S., Schwall, R., Sinicropi, D. & Ashkenazi, A. (2002) Tumor-cell resistance to death receptor-induced apoptosis through mutational inactivation of the proapoptotic Bcl-2 homolog Bax. Nat. Med. 8, 274-281.
25. Luo, X., Budihardjo, I., Zuo, H., Slaughter, C. & Want, X. (1998) Bid, a Bcl-2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94, 481-490.
26. Berenbaum, M.C. (1978) A method for testing for synergy with any number of agents. J. Infect. Dis. 137, 122-130.
27. Samuel, C., Cheng, S., Dan, L. & Yong, X. (2001) Taxol induced Bcl-2 protein phosphorylation in human hepatocellular carcinoma QGY-7703 cell line. Cell Biol. Int. 25, 261-265.
28. Jo, M., Kim, T.H., Seol, D.W., Esplen, J.E., Dorko, K., Billiar, T.R. & Strom, S.C. (2000) Apoptosis induced in normal human hepatocytes by tumor necrosis factor-related apoptosis-inducing ligand. Nat. Med. 6, 564-567.
29. Munshi, A., McDonnell, T.J. & Meyn, R.E. (2002) Chemotherapeutic agents enhance TRAIL-induced apoptosis in prostate cancer cells. Cancer Chemother. Pharmacol. 50, 46-52.
30. Maccon, M.K., Ettenberg, S.A., Nau, M.M., Russell, E.K. & Lipkowitz, S. (1999) Chemotherapy augments TRAIL-induced apoptosis in breast cell lines. Cancer Res. 59, 734-741.
31. Scott, H.K. & William, C.E. (2000) Induction of apoptosis by cancer chemotherapy. Exp. Cell Res. 256, 42-49.
32. Karpinich, N.O., Tafani, M., Rothman, R.J., Russo, M.A. & Farber, J.L. (2002) The course of etoposide-induced apoptosis from damage to DNA and p53 activation to mitochondrial release of cytochrome c. J. Biol. Chem. 277, 16547-16552.
33. Rieger, J., Naumann, U., Glaser, T., Ashkenazi, A. & Weller, M. (1998) Apo2 ligand: a novel lethal weapon against malignant glioma? FEBS Lett. 427, 124-128.
34. Miyashita, T. & Reed, J.C. (1995) Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80, 293-299.
35. Wu, G.S., Burns, T.F., McDonald, E.R., Jiang, W., Meng, R., Krantz, I.D., Kao, G., Gan, D.D., Zhou, J.Y., Muschel, R., Hamilton, S.R., Spinner, N.B., Markowitz, S., Wu, G. & El-Deiry, W.S. (1997) KILLER/DR5 is a DNA damage-inducible p53-regulated death receptor gene. Nat. Genet. 17, 141-143.
36. Baoxiang, G., Ping, Y., Gary, L.C. & Sun, S.Y. (2001) Evidence that the death receptor DR4 is a DNA damage-inducible, p53-regulated gene. J. Cell. Physiol. 188, 98-105.
37. Raymond, D.M., McDonald, E.R., Sheikh, M.S., Albert, J.F. & Wafik, S. (2000) The TRAIL decoy receptor TRUNDD (DcR2, TRAIL-R4) is induced by adenovirus-p53 overexpression and can delay TRAIL-, p53-, and KILLER/DR5-dependent colon cancer apoptosis. Mol. Ther. 1, 130-144.
38. Shi, Y.S., Yue, P., Hong, W.K. & Lotan, R. (2000) Augmentation of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis by the synthetic retinoid 6-[3-(1-Adamantyl)-4-hydroxyphenyl]-2-naphthalene carboxylic acid (CD437) through up-regulation of TRAIL receptors in human lung cancer cells. Cancer Res. 60, 7149-7155.
39. Sheikh, M.S., Burns, T.F., Huang, Y., Wu, G.S., Amundson, S., Brooks, K.S., Fornace, A.J. Jr, & el-Deiry, W.S. (1998) p53-dependent and -independent regulation of the death receptor KILLER/DR5 gene expression in response to genotoxic stress and tumor necrosis factor alpha. Cancer Res. 58, 1593-1598.
40. Liu, W., Bodle, E., Chen, J.Y., Gao, M., Rosen, G.D. & Broaddus, V.C. (2001) Tumor necrosis factor-related apoptosis-inducing ligand and chemotherapy cooperate to induce apoptosis in mesothelioma cell lines. Am. J. Respir. Cell Mol. Biol. 25, 111-118.
41. Sax, J.K., Fei, P., Murphy, M.E., Bernhard, E., Korsmeyer, S.J. & Walfik, S.E.-D. (2002) BID regulation by p53 contributes to chemosensitivity. Nat. Cell Biol. 4, 842-849.
42. 6- Methylguanine is Bcl-2 and caspase-9/3 regulated and Fas/caspase-8 independent. Cancer Res. 60, 5815-5824.
43. Korsmeyer, S.J., Wei, M.C., Saito, M., Weiler, S., Oh, K.J. & Schlesinger, P.H. (2000) Pro-apoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c. Cell Death Differ. 7, 1166-1173.
44. Li, H., Zhu, H., Xu, C.J. & Yuan, J. (1998) Cleavage of BID by caspase8 mediated the mitochondria in response to activation of cell surface death receptors. Cell 94, 491-450.
45. Kim, J.Y., Kim, Y.H., Chang, I., Kim, S., Pak, Y.K., Oh, B.H., Yagita, H., Jung, Y.K., Oh, Y.J. & Lee, M.S. (2002) Resistance of mitochondrial DNA-deficient cells to TRAIL: role of Bax in TRAIL-induced apoptosis. Oncogene 21, 3139-3148.
46. Green, D.R. & Reed, J.C. (1998) Mitochondria and apoptosis. Science 281, 130-1312.
47. Ruth, M.K., Ella, B.-W., Douglas, R.G. & Donald, D.N. (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275, 1132-1136.
48. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S.M., Ahmad, M., Alnemri, E.S. & Wang, X. (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91, 479-489.
49. Dn, C., Fang, M., Li, Y. & Wang, X. (2000) Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102, 33-42.
50. Ekert, P.G., Silke, J., Hawkins, C.J., Verhagen, A.M. & Vaux, D.L. (2001) DIABLO promotes apoptosis by removing MIHA/XIAP from processed caspase9. J. Cell Biol. 152, 483-490.
51. Yibin, D., Yahong, L. & Xiang, W.W. (2002) TRAIL-induced apoptosis requires Bax-dependent mitochondrial release of Smac/DIABLO. Genes Dev. 16, 33-45.
52. Adrain, C., Creagh, E.M. & Martin, S.J. (2001) Apoptosis-associated release of Smac/DIABLO from mitochondria requires active caspases and is blocked by Bcl-2. EMBO J. 20, 6627-6636.
53. Engel, I.H., Strpczynska, A., Stroh, C., Lauber, K., Berg, C., Schwenzer, R., Wajant, H., Janicke, R.U., Porter, A.G., Belka, C., Gregor, M., Schulze, O.K. & Wesselborg, S. (2000) Caspase-8/FLICE functions as an executioner caspase in anticancer drug-induced apoptosis. Oncogene 19, 4563-4573.
54. Wesselborg, S., Engel, I.H., Rossmann, E., Los, M. & Schulze, O.K. (1999) Anticancer drugs induce caspase-8/FLICE activation and apoptosis in the absence of CD95 receptor/ligand interation. Blood 93, 3053-3063.
55. Nancy, A., Thornberry, N.A. & Yuri, L. (1998) Caspases: enemies within. Science 281, 1312-1316.
56. Sun, X.M., MacFarlane, M., Zhuang, J., Wolf, B.B., Green, D.R. & Cohen, G.M. (1999) Distinct caspase cascades are initiated in receptor-mediated and chemical-induced apoptosis. J. Biol. Chem. 274, 5053-5060.