Enhanced caspase-8 recruitment to and activation at the disc is critical for sensitisation of human hepatocellular carcinoma cells to trail-induced apoptosis by chemotherapeutic drugs

Cell Death and Differentiation

Volumn 11, Issue , 2004, Pages S86-S96

  Ganten, T M ^a,b   Haas, T L ^a   Sykora, J ^a,b   Stahl, H ^a   Sprick, M R ^a   Fas, S C ^a   Krueger, A ^a   Weigand, M A ^a   Grosse Wilde, A ^a   Stremmel, W ^b   Krammer, P H ^a   Walczak, H ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Cflip sirna death receptor; Death inducing signalling complex disc; Drug sensitivity; Hepatocellular carcinoma; Trail

Indexed keywords

ANTINEOPLASTIC AGENT; CASPASE 8; CELL PROTEIN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; FLICE INHIBITORY PROTEIN; FLUOROURACIL; PROTEIN DISC; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG SENSITIZATION; ENZYME ACTIVATION; ENZYME MECHANISM; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; PRIORITY JOURNAL; PROTEIN ANALYSIS; SENSITIVITY ANALYSIS; TUMOR CELL LINE; TUMOR RESISTANCE; UPREGULATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANTIBODIES, MONOCLONAL; ANTIGENS, CD95; ANTINEOPLASTIC AGENTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BLOTTING, WESTERN; CARCINOMA, HEPATOCELLULAR; CASP8 AND FADD-LIKE APOPTOSIS REGULATING PROTEIN; CASPASE 3; CASPASE 6; CASPASE 8; CASPASES; CELL LINE, TUMOR; CELL SURVIVAL; DEATH DOMAIN RECEPTOR SIGNALING ADAPTOR PROTEINS; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; ENZYME PRECURSORS; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; FLOW CYTOMETRY; FLUOROURACIL; GREEN FLUORESCENT PROTEINS; HEPATOCYTES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER NEOPLASMS; MEMBRANE GLYCOPROTEINS; MICROSCOPY, FLUORESCENCE; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; RECEPTORS, TUMOR NECROSIS FACTOR; RECOMBINANT FUSION PROTEINS; RNA, SMALL INTERFERING; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TRANSFECTION; TUMOR NECROSIS FACTOR DECOY RECEPTORS; TUMOR NECROSIS FACTOR-ALPHA; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 4344607589     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/sj.cdd.4401437     Document Type: Article

References (73)

1. Wiley SR, Smolak PJ, Din WS, Huang CP, Nicholl JK, Sutherland GR, Smith TD, Rauch C and Smith CA (1995) Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 3: 673-682
2. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, Kubin M, Chin W, Jones J, Woodward A, Le T, Smith C, Smolak P, Goodwin RG, Rauch CT, Schuh JC and Lynch DH (1999) Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat. Med. 5: 157-163
3. Gores GJ and Kaufmann SH (2001) Is TRAIL hepatotoxic? Hepatology 34: 3-6
4. Ashkenazi A, Pai RC, Fong S, Leung S, Lawrence DA, Marsters SA, Blackie C, Chang L, McMurtrey AE, Hebert A, DeForge L, Koumenis IL, Lewis D, Harris L, Bussiere J, Koeppen H, Shahrokh Z and Schwall RH (1999) Safety and antitumor activity of recombinant soluble Apo2 ligand. J. Clin. Invest. 104: 155-162
5. Gliniak B and Le T (1999) Tumor necrosis factor-related apoptosis-inducing ligand’s antitumor activity in vivo is enhanced by the chemotherapeutic agent CPT-11. Cancer Res. 59: 6153-6158
6. Jo M, Kim TH, Seol DW, Esplen JE, Dorko K, Billiar TR and Strom SC (2000) Apoptosis induced in normal human hepatocytes by tumor necrosis factorrelated apoptosis-inducing ligand. Nat. Med. 6: 564-567
7. Ichikawa K, Liu W, Zhao L, Wang Z, Liu D, Ohtsuka T, Zhang H, Mountz JD, Koopman WJ, Kimberly RP and Zhou T (2001) Tumoricidal activity of a novel anti-human DR5 monoclonal antibody without hepatocyte cytotoxicity. Nat. Med. 7: 954-960
8. Lawrence D, Shahrokh Z, Marsters S, Achilles K, Shih D, Mounho B, Hillan K, Totpal K, DeForge L, Schow P, Hooley J, Sherwood S, Pai R, Leung S, Khan L, Gliniak B, Bussiere J, Smith CA, Strom SS, Kelley S, Fox JA, Thomas D and Ashkenazi A (2001) Differential hepatocyte toxicity of recombinant Apo2L/TRAIL versions. Nat. Med. 7: 383-385
9. Pan G, O’Rourke K, Chinnaiyan AM, Gentz R, Ebner R, Ni J and Dixit VM (1997) The receptor for the cytotoxic ligand TRAIL. Science 276: 111-113
10. Schneider P, Bodmer JL, Thome M, Hofmann K, Holler N and Tschopp J (1997) Characterization of two receptors for TRAIL. FEBS Lett. 416: 329-334
11. Walczak H, Degli-Esposti MA, Johnson RS, Smolak PJ, Waugh JY, Boiani N, Timour MS, Gerhart MJ, Schooley KA Smith CA, Goodwin RG and Rauch CT (1997) TRAIL-R2: a novel apoptosis-mediating receptor for TRAIL. EMBO J. 16: 5386-5397
12. Sheridan JP, Marsters SA, Pitti RM, Gurney A, Skubatch M, Baldwin D, Ramakrishnan L, Gray CL, Baker K, Wood WI, Goddard AD, Godowski P and Ashkenazi A (1997) Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 277: 818-821
13. Wu GS, Burns TF, McDonald III ER, Jiang W, Meng R, Krantz ID, Kao G, Gan DD, Zhou JY, Muschel R, Hamilton SR, Spinner NB, Markowitz S, Wu G and el- Deiry WS (1997) KILLER/DR5 is a DNA damage-inducible p53-regulated death receptor gene. Nat. Genet. 17: 141-143
14. Screaton GR, Mongkolsapaya J, Xu XN, Cowper AE, McMichael AJ and Bell JI (1997) TRICK2, a new alternatively spliced receptor that transduces the cytotoxic signal from TRAIL. Curr. Biol. 7: 693-696
15. MacFarlane M, Ahmad M, Srinivasula SM, Fernandes-Alnemri T, Cohen GM and Alnemri ES (1997) Identification and molecular cloning of two novel receptors for the cytotoxic ligand TRAIL. J. Biol. Chem. 272: 25417-25420
16. Krammer PH (2000) CD95’s deadly mission in the immune system. Nature 407: 789-795
17. Peter ME, Scaffidi C, Medema JP, Kischkel F and Krammer PH (1999) The death receptors. Results Probl. Cell Differ. 23: 25-63
18. Degli-Esposti MA, Smolak PJ, Walczak H, Waugh J, Huang CP, DuBose RF, Goodwin RG and Smith CA (1997) Cloning and characterization of TRAIL-R3, a novel member of the emerging TRAIL receptor family. J. Exp. Med. 186: 1165-1170
19. Pan G, Ni J, Yu G, Wei YF and Dixit VM (1998) TRUNDD, a new member of the TRAIL receptor family that antagonizes TRAIL signalling. FEBS Lett. 424: 41-45
20. Mongkolsapaya J, Cowper AE, Xu XN, Morris G, McMichael AJ, Bell JI and Screaton GR (1998) Lymphocyte inhibitor of TRAIL (TNF-related apoptosisinducing ligand): a new receptor protecting lymphocytes from the death ligand TRAIL. J. Immunol. 160: 3-6
21. Degli-Esposti MA, Dougall WC, Smolak PJ, Waugh JY, Smith CA and Goodwin RG (1997) The novel receptor TRAIL-R4 induces NF-kappaB and protects against TRAIL-mediated apoptosis, yet retains an incomplete death domain. Immunity 7: 813-820
22. Emery JG, McDonnell P, Burke MB, Deen KC, Lyn S, Silverman C, Dul E, Appelbaum ER, Eichman C, DiPrinzio R, Dodds RA, James IE, Rosenberg M, Lee JC and Young PR (1998) Osteoprotegerin is a receptor for the cytotoxic ligand TRAIL. J. Biol. Chem. 273: 14363-14367
23. Walczak H and Sprick MR (2001) Biochemistry and function of the DISC. Trends Biochem. Sci. 26: 452-453
24. Sprick MR, Weigand MA, Rieser E, Rauch CT, Juo P, Blenis J, Krammer PH and Walczak H (2000) FADD/MORT1 and caspase-8 are recruited to TRAIL receptors 1 and 2 and are essential for apoptosis mediated by TRAIL receptor Immunity 12: 599-609
25. Kischkel FC, Lawrence DA, Chuntharapai A, Schow P, Kim KJ and Ashkenazi A (2000) Apo2L/TRAIL-dependent recruitment of endogenous FADD and caspase-8 to death receptors 4 and 5. Immunity 12: 611-620
26. Bodmer JL, Holler N, Reynard S, Vinciguerra P, Schneider P, Juo P, Blenis J and Tschopp J (2000) TRAIL receptor-2 signals apoptosis through FADD and caspase-8. Nat. Cell Biol. 2: 241-243
27. Sprick MR, Rieser E, Stahl H, Grosse-Wilde A, Weigand MA and Walczak H (2002) Caspase-10 is recruited to and activated at the native TRAIL and CD95 death-inducing signalling complexes in a FADD-dependent manner but cannot functionally substitute caspase-8. EMBO J. 21: 4520-4530
28. Kischkel FC, Lawrence DA, Tinel A, LeBlanc H, Virmani A, Schow P, Gazdar A, Blenis J, Arnott D and Ashkenazi A (2001) Death receptor recruitment of endogenous caspase-10 and apoptosis initiation in the absence of caspase-8. J. Biol. Chem. 276: 46639-46646
29. Cuello M, Ettenberg SA, Nau MM and Lipkowitz S (2001) Synergistic induction of apoptosis by the combination of trail and chemotherapy in chemoresistant ovarian cancer cells. Gynecol. Oncol. 81: 380-390
30. Lacour S, Hammann A, Wotawa A, Corcos L, Solary E and Dimanche-Boitrel MT (2001) Anticancer agents sensitize tumor cells to tumor necrosis factorrelated apoptosis-inducing ligand-mediated caspase-8 activation and apoptosis. Cancer Res. 61: 1645-1651
31. Nagane M, Pan G, Weddle JJ, Dixit VM, Cavenee WK and Huang HJ (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. 60: 847-853
32. Houghton JA (1999) Apoptosis and drug response. Curr. Opin. Oncol. 11: 475-481
33. Belka C, Schmid B, Marini P, Durand E, Rudner J, Faltin H, Bamberg M, Schulze-Osthoff K and Budach W (2001) Sensitization of resistant lymphoma cells to irradiation-induced apoptosis by the death ligand TRAIL. Oncogene 20: 2190-2196
34. Zhang XD, Nguyen T, Thomas WD, Sanders JE and Hersey P (2000) Mechanisms of resistance of normal cells to TRAIL induced apoptosis vary between different cell types. FEBS Lett. 482: 193-199
35. Wen J, Ramadevi N, Nguyen D, Perkins C, Worthington E and Bhalla K (2000) Antileukemic drugs increase death receptor 5 levels and enhance Apo- 2L-induced apoptosis of human acute leukemia cells. Blood 96: 3900-3906
36. Thomas WD, Zhang XD, Franco AV, Nguyen T and Hersey P (2000) TNFrelated apoptosis-inducing ligand-induced apoptosis of melanoma is associated with changes in mitochondrial membrane potential and perinuclear clustering of mitochondria. J. Immunol. 165: 5612-5620
37. van Noesel MM, van Bezouw S, Salomons GS, Voute PA, Pieters R, Baylin SB, Herman JG and Versteeg R (2002) Tumor-specific down-regulation of the tumor necrosis factor-related apoptosis-inducing ligand decoy receptors DcR1 and DcR2 is associated with dense promoter hypermethylation. Cancer Res. 62: 2157-2161
38. Spalding AC, Jotte RM, Scheinman RI, Geraci MW, Clarke P, Tyler KL and Johnson GL (2002) TRAIL and inhibitors of apoptosis are opposing determinants for NF-kappaB-dependent, genotoxin-induced apoptosis of cancer cells. Oncogene 21: 260-271
39. Leaman DW, Chawla-Sarkar M, Vyas K, Reheman M, Tamai K, Toji S and Borden EC (2002) Identification of X-linked inhibitor of apoptosis-associated factor-1 as an interferon-stimulated gene that augments TRAIL Apo2L-induced apoptosis. J. Biol. Chem. 277: 28504-28511
40. Kim JY, Kim YH, Chang I, Kim S, Pak YK, Oh BH, Yagita H, Jung YK, Oh YJ and Lee MS (2002) Resistance of mitochondrial DNA-deficient cells to TRAIL: role of Bax in TRAIL-induced apoptosis. Oncogene 21: 3139-3148
41. Walczak H, Bouchon A, Stahl H and Krammer PH (2000) Tumor necrosis factor-related apoptosis-inducing ligand retains its apoptosis-inducing capacity on Bcl-2- or Bcl-xL-overexpressing chemotherapy-resistant tumor cells. Cancer Res. 60: 3051-3057
42. Bernard D, Quatannens B, Vandenbunder B and Abbadie C (2001) Rel/NFkappaB transcription factors protect against tumor necrosis factor (TNF)-related apoptosis-inducing ligand (TRAIL)-induced apoptosis by up-regulating the TRAIL decoy receptor DcR1. J. Biol. Chem. 276: 27322-27328
43. Leverkus M, Neumann M, Mengling T, Rauch CT, Brocker EB, Krammer PH and Walczak H (2000) Regulation of tumor necrosis factor-related apoptosisinducing ligand sensitivity in primary and transformed human keratinocytes. Cancer Res. 60: 553-559
44. Hao C, Beguinot F, Condorelli G, Trencia A, Van Meir EG, Yong VW, Parney IF, Roa WH and Petruk KC (2001) Induction and intracellular regulation of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) mediated apoptosis in human malignant glioma cells. Cancer Res. 61: 1162-1170
45. Chang DW, Xing Z, Pan Y, Algeciras-Schimnich A, Barnhart BC, Yaish-Ohad S, Peter ME and Yang X (2002) c-FLIP(L) is a dual function regulator for caspase-8 activation and CD95-mediated apoptosis. EMBO J. 21: 3704-3714
46. Yamanaka T, Shiraki K, Sugimoto K, Ito T, Fujikawa K, Ito M, Takase K, Moriyama M, Nakano T and Suzuki A (2000) Chemotherapeutic agents augment TRAIL-induced apoptosis in human hepatocellular carcinoma cell lines. Hepatology 32: 482-490
47. Muller M, Scaffidi CA, Galle PR, Stremmel W and Krammer PH (1998) The role of p53 and the CD95 (APO-1/Fas) death system in chemotherapy-induced apoptosis. Eur. Cytokine Network 9: 685-686
48. Krueger A, Schmitz I, Baumann S, Krammer PH and Kirchhoff S (2001) Cellular FLICE-inhibitory protein splice variants inhibit different steps of caspase-8 activation at the cd95 death-inducing signaling complex. J. Biol. Chem. 276: 20633-20640
49. Irmler M, Thome M, Hahne M, Schneider P, Hofmann K, Steiner V, Bodmer JL, Schroter M, Burns K, Mattmann C, Rimoldi D, French LE and Tschopp J (1997) Inhibition of death receptor signals by cellular FLIP. Nature 388: 190-195
50. Siegmund D, Hadwiger P, Pfizenmaier K, Vornlocher HP and Wajant H (2002) Selective inhibition of FLICE-like inhibitory protein expression with small interfering RNA oligonucleotides is sufficient to sensitize tumor cells for TRAILinduced apoptosis. Mol. Med. 8: 725-732
51. Higuchi H, Bronk SF, Takikawa Y, Werneburg N, Takimoto R, El-Deiry W and Gores GJ (2001) The bile acid glycochenodeoxycholate induces TRAILreceptor 2/DR5 expression and apoptosis. J. Biol. Chem. 276: 38610-38618
52. Guan B, Yue P, Clayman GL and Sun SY (2001) Evidence that the death receptor DR4 is a DNA damage-inducible, p53-regulated gene. J. Cell. Physiol. 188: 98-105
53. Kastan M (1997) On the TRAIL from p53 to apoptosis? Nat. Genet. 17: 130-131
54. Sheikh MS, Burns TF, Huang Y, Wu GS, Amundson S, Brooks KS, Fornace AJ, Jr and el-Deiry WS (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
55. Sheikh MS, Fornace AJ and Jr (2000) Death and decoy receptors and p53- mediated apoptosis. Leukemia 14: 1509-1513
56. Wu WG, Soria JC, Wang L, Kemp BL and Mao L (2000) TRAIL-R2 is not correlated with p53 status and is rarely mutated in non-small cell lung cancer. Anticancer Res. 20: 4525-4529
57. Deng Y, Lin Y and Wu X (2002) TRAIL-induced apoptosis requires Bax-dependent mitochondrial release of Smac/DIABLO. Genes Dev. 16: 33-45
58. Leverkus M, Sprick MR, Wachter T, Mengling T, Baumann B, Serfling E, Brocker EB, Goebeler M, Neumann M and Walczak H (2003) Proteasome inhibition results in TRAIL sensitization of primary keratinocytes by removing the resistance-mediating block of effector caspase maturation. Mol. Cell. Biol. 23: 777-790
59. Fulda S, Wick W, Weller M and Debatin KM (2002) Smac agonists sensitize for Apo2L/TRAIL- or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat. Med. 8: 808-815
60. Zhang XD, Zhang XY, Gray CP, Nguyen T and Hersey P (2001) Tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis of human melanoma is regulated by Smac/DIABLO release from mitochondria. Cancer Res. 61: 7339-7348
61. Fulda S, Meyer E and Debatin KM (2002) Inhibition of TRAIL-induced apoptosis by Bcl-2 overexpression. Oncogene 21: 2283-2294
62. Bin L, Li X, Xu LG and Shu HB (2002) The short splice form of Casper/c-FLIP is a major cellular inhibitor of TRAIL-induced apoptosis. FEBS Lett. 510: 37-40
63. Thome M, Schneider P, Hofmann K, Fickenscher H, Meinl E, Neipel F, Mattmann C, Burns K, Bodmer JL, Schroter M, Scaffidi C, Krammer PH, Peter ME and Tschopp J (1997) Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 386: 517-521
64. Scaffidi C, Schmitz I, Krammer PH and Peter ME (1999) The role of c-FLIP in modulation of CD95-induced apoptosis. J. Biol. Chem. 274: 1541-1548
65. Kirchhoff S, Muller WW, Krueger A, Schmitz I and Krammer PH (2000) TCRmediated up-regulation of c-FLIP short correlates with resistance toward CD95- mediated apoptosis by blocking death-inducing signaling complex activity. J. Immunol. 165: 6293-6300
66. Harper N, Farrow SN, Kaptein A, Cohen GM and MacFarlane M (2001) Modulation of tumor necrosis factor apoptosis-inducing ligand-induced NF-kappa B activation by inhibition of apical caspases. J. Biol. Chem. 276: 34743-34752
67. Griffith TS, Chin WA, Jackson GC, Lynch DH and Kubin MZ (1998) Intracellular regulation of TRAIL-induced apoptosis in human melanoma cells. J. Immunol. 161: 2833-2840
68. Suliman A, Lam A, Datta R and Srivastava RK (2001) Intracellular mechanisms of TRAIL: apoptosis through mitochondrial-dependent and -independent pathways. Oncogene 20: 2122-2133
69. Srivastava RK (2000) Intracellular mechanisms of TRAIL and its role in cancer therapy. Mol. Cell. Biol. Res. Commun. 4: 67-75
70. MacFarlane M, Harper N, Snowden RT, Dyer MJ, Barnett GA, Pringle JH and Cohen GM (2002) Mechanisms of resistance to TRAIL-induced apoptosis in primary B cell chronic lymphocytic leukaemia. Oncogene 21: 6809-6818
71. Scaffidi C, Medema JP, Krammer PH and Peter ME (1997) FLICE is predominantly expressed as two functionally active isoforms, caspase-8/a and caspase-8/b. J. Biol. Chem. 272: 26953-26958
72. Nicoletti I, Migliorati G, Pagliacci MC, Grignani F and Riccardi C (1991) A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 139: 271-279
73. Zhang L, Fogg DK and Waisman DM (2003) RNA interference-mediated silencing of the S100A10 genattenuates plasmin generation and invasiveness of Colo 222 colorectal cancer cells. J. Biol. Chem. 279: 2053-2062