Proapoptotic DR4 and DR5 signaling in cancer cells: Toward clinical translation

Current Opinion in Cell Biology

Volumn 22, Issue 6, 2010, Pages 837-844

  Yang, Annie ^a   Wilson, Nicholas S ^a   Ashkenazi, Avi ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BORTEZOMIB; DEATH RECEPTOR 4; DEATH RECEPTOR 5; DECOY RECEPTOR 3; DULANERMIN; HISTONE DEACETYLASE INHIBITOR; MONOCLONAL ANTIBODY; PROAPOPTOTIC RECEPTOR AGONIST; SORAFENIB; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER INHIBITION; CANCER THERAPY; CLINICAL TRIAL; DRUG EFFICACY; DRUG SENSITIVITY; DRUG TOLERABILITY; HUMAN; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA TRANSLATION; TUMOR CELL; UPREGULATION;

ANIMALS; APOPTOSIS; CELL MEMBRANE; HUMANS; MITOCHONDRIA; NEOPLASMS; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; SIGNAL TRANSDUCTION; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 78649634124     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2010.08.001     Document Type: Review

References (70)

1. Brenner D., Mak T.W. Mitochondrial cell death effectors. Curr Opin Cell Biol 2009, 21:871-877.
2. Vaux D.L., Silke J. IAPs, RINGs and ubiquitylation. Nat Rev Mol Cell Biol 2005, 6:287-297.
3. Wilson N.S., Dixit V., Ashkenazi A. Death receptor signal transducers: nodes of coordination in immune signaling networks. Nat Immunol 2009, 10:348-355.
4. Gonzalvez F., Ashkenazi A. New insights into apoptosis signaling by Apo2L/TRAIL. Oncogene 2010, 29:4752-4765.
5. Daniel D., Wilson N.S. Tumor necrosis factor: renaissance as a cancer therapeutic?. Curr Cancer Drug Targets 2008, 8:124-131.
6. Ashkenazi A. Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nat Rev Cancer 2002, 2:420-430.
7. Ashkenazi A. Directing cancer cells to self-destruct with pro-apoptotic receptor agonists. Nat Rev Drug Discov 2008, 7:1001-1012.
8. Johnstone R.W., Frew A.J., Smyth M.J. The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat Rev Cancer 2008, 8:782-798.
9. Yue H.H., Diehl G.E., Winoto A. Loss of TRAIL-R does not affect thymic or intestinal tumor development in p53 and adenomatous polyposis coli mutant mice. Cell Death Differ 2005, 12:94-97.
10. Dunn G.P., Koebel C.M., Schreiber R.D. Interferons, immunity and cancer immunoediting. Nat Rev Immunol 2006, 6:836-848.
11. Cretney E., Takeda K., Yagita H., Glaccum M., Peschon J.J., Smyth M.J. Increased susceptibility to tumor initiation and metastasis in TNF-related apoptosis-inducing ligand-deficient mice. J Immunol 2002, 168:1356-1361.
12. Takeda K., Smyth M.J., Cretney E., Hayakawa Y., Kayagaki N., Yagita H., Okumura K. Critical role for tumor necrosis factor-related apoptosis-inducing ligand in immune surveillance against tumor development. J Exp Med 2002, 195:161-169.
13. Wiezorek J., Holland P., Graves J. Death receptor agonists as a targeted therapy for cancer. Clin Cancer Res 2010, 16:1701-1708.
14. Wagner K.W., Punnoose E.A., Januario T., Lawrence D.A., Pitti R.M., Lancaster K., Lee D., von Goetz M., Yee S.F., Totpal K., et al. Death-receptor O-glycosylation controls tumor-cell sensitivity to the proapoptotic ligand Apo2L/TRAIL. Nat Med 2007, 13:1070-1077.
15. Naka T., Sugamura K., Hylander B.L., Widmer M.B., Rustum Y.M., Repasky E.A. Effects of tumor necrosis factor-related apoptosis-inducing ligand alone and in combination with chemotherapeutic agents on patients' colon tumors grown in SCID mice. Cancer Res 2002, 62:5800-5806.
16. Cheng J., Hylander B.L., Baer M.R., Chen X., Repasky E.A. Multiple mechanisms underlie resistance of leukemia cells to Apo2 Ligand/TRAIL. Mol Cancer Ther 2006, 5:1844-1853.
17. Hylander B.L., Pitoniak R., Penetrante R.B., Gibbs J.F., Oktay D., Cheng J., Repasky E.A. The anti-tumor effect of Apo2L/TRAIL on patient pancreatic adenocarcinomas grown as xenografts in SCID mice. J Transl Med 2005, 3:22.
18. 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., et al. Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 1997, 277:818-821.
19. Ichikawa K., Liu W., Zhao L., Wang Z., Liu D., Ohtsuka T., Zhang H., Mountz J.D., Koopman W.J., Kimberly R.P., et al. Tumoricidal activity of a novel anti-human DR5 monoclonal antibody without hepatocyte cytotoxicity. Nat Med 2001, 7:954-960.
20. Brincks E.L., Katewa A., Kucaba T.A., Griffith T.S., Legge K.L. CD8 T cells utilize TRAIL to control influenza virus infection. J Immunol 2008, 181:4918-4925.
21. Pennarun B., Meijer A., de Vries E.G., Kleibeuker J.H., Kruyt F., de Jong S. Playing the DISC: turning on TRAIL death receptor-mediated apoptosis in cancer. Biochim Biophys Acta 2010, 1805:123-140.
22. Ozoren N., El-Deiry W.S. Cell surface death receptor signaling in normal and cancer cells. Semin Cancer Biol 2003, 13:135-147.
23. Bin L., Thorburn J., Thomas L.R., Clark P.E., Humphreys R., Thorburn A. Tumor-derived mutations in the TRAIL receptor DR5 inhibit TRAIL signaling through the DR4 receptor by competing for ligand binding. J Biol Chem 2007, 282:28189-28194.
24. Elias A., Siegelin M.D., Steinmuller A., von Deimling A., Lass U., Korn B., Mueller W. Epigenetic silencing of death receptor 4 mediates tumor necrosis factor-related apoptosis-inducing ligand resistance in gliomas. Clin Cancer Res 2009, 15:5457-5465.
25. Horak P., Pils D., Haller G., Pribill I., Roessler M., Tomek S., Horvat R., Zeillinger R., Zielinski C., Krainer M. Contribution of epigenetic silencing of tumor necrosis factor-related apoptosis inducing ligand receptor 1 (DR4) to TRAIL resistance and ovarian cancer. Mol Cancer Res 2005, 3:335-343.
26. Bae S.I., Cheriyath V., Jacobs B.S., Reu F.J., Borden E.C. Reversal of methylation silencing of Apo2L/TRAIL receptor 1 (DR4) expression overcomes resistance of SK-MEL-3 and SK-MEL-28 melanoma cells to interferons (IFNs) or Apo2L/TRAIL. Oncogene 2008, 27:490-498.
27. Stern H.M., Padilla M., Wagner K., Amler L., Ashkenazi A. Development of immunohistochemistry assays to assess GALNT14 and FUT3/6 in clinical trials of dulanermin and drozitumab. Clin Cancer Res 2010, 16:1587-1596.
28. Rossin A., Derouet M., Abdel-Sater F., Hueber A.O. Palmitoylation of the TRAIL receptor DR4 confers an efficient TRAIL-induced cell death signalling. Biochem J 2009, 419. 185-192, 182 p following 192.
29. Tang Z., Bauer J.A., Morrison B., Lindner D.J. Nitrosylcobalamin promotes cell death via S nitrosylation of Apo2L/TRAIL receptor DR4. Mol Cell Biol 2006, 26:5588-5594.
30. Schutze S., Tchikov V., Schneider-Brachert W. Regulation of TNFR1 and CD95 signalling by receptor compartmentalization. Nat Rev Mol Cell Biol 2008.
31. Jin Z., McDonald E.R., Dicker D.T., El-Deiry W.S. Deficient tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) death receptor transport to the cell surface in human colon cancer cells selected for resistance to TRAIL-induced apoptosis. J Biol Chem 2004, 279:35829-35839.
32. Zhang Y., Zhang B. TRAIL resistance of breast cancer cells is associated with constitutive endocytosis of death receptors 4 and 5. Mol Cancer Res 2008, 6:1861-1871.
33. Greco F.A., Bonomi P., Crawford J., Kelly K., Oh Y., Halpern W., Lo L., Gallant G., Klein J. Phase 2 study of mapatumumab, a fully human agonistic monoclonal antibody which targets and activates the TRAIL receptor-1, in patients with advanced non-small cell lung cancer. Lung Cancer 2008, 61:82-90.
34. Trarbach T., Moehler M., Heinemann V., Kohne C.H., Przyborek M., Schulz C., Sneller V., Gallant G., Kanzler S. Phase II trial of mapatumumab, a fully human agonistic monoclonal antibody that targets and activates the tumour necrosis factor apoptosis-inducing ligand receptor-1 (TRAIL-R1), in patients with refractory colorectal cancer. Br J Cancer 2010, 102:506-512.
35. Kelley R.F., Totpal K., Lindstrom S.H., Mathieu M., Billeci K., Deforge L., Pai R., Hymowitz S.G., Ashkenazi A. Receptor-selective mutants of apoptosis-inducing ligand 2/tumor necrosis factor-related apoptosis-inducing ligand reveal a greater contribution of death receptor (DR) 5 than DR4 to apoptosis signaling. J Biol Chem 2005, 280:2205-2212.
36. MacFarlane M., Inoue S., Kohlhaas S.L., Majid A., Harper N., Kennedy D.B., Dyer M.J., Cohen G.M. Chronic lymphocytic leukemic cells exhibit apoptotic signaling via TRAIL-R1. Cell Death Differ 2005, 12:773-782.
37. LeBlanc H.N., Ashkenazi A. Apo2L/TRAIL and its death and decoy receptors. Cell Death Differ 2003, 10:66-75.
38. Clancy L., Mruk K., Archer K., Woelfel M., Mongkolsapaya J., Screaton G., Lenardo M.J., Chan F.K. Preligand assembly domain-mediated ligand-independent association between TRAIL receptor 4 (TR4) and TR2 regulates TRAIL-induced apoptosis. Proc Natl Acad Sci U S A 2005, 102:18099-18104.
39. Merino D., Lalaoui N., Morizot A., Schneider P., Solary E., Micheau O. Differential inhibition of TRAIL-mediated DR5-DISC formation by decoy receptors 1 and 2. Mol Cell Biol 2006, 26:7046-7055.
40. Muppidi J.R., Tschopp J., Siegel R.M. Life and death decisions: secondary complexes and lipid rafts in TNF receptor family signal transduction. Immunity 2004, 21:461-465.
41. Budd R.C., Yeh W.C., Tschopp J. cFLIP regulation of lymphocyte activation and development. Nat Rev Immunol 2006, 6:196-204.
42. Sharp D.A., Lawrence D.A., Ashkenazi A. Selective knockdown of the long variant of cellular FLICE inhibitory protein augments death receptor-mediated caspase-8 activation and apoptosis. J Biol Chem 2005, 280:19401-19409.
43. Golks A., Brenner D., Krammer P.H., Lavrik I.N. The c-FLIP-NH2 terminus (p22-FLIP) induces NF-kappaB activation. J Exp Med 2006, 203:1295-1305.
44. Song J.H., Tse M.C., Bellail A., Phuphanich S., Khuri F., Kneteman N.M., Hao C. Lipid rafts and nonrafts mediate tumor necrosis factor related apoptosis-inducing ligand induced apoptotic and nonapoptotic signals in non small cell lung carcinoma cells. Cancer Res 2007, 67:6946-6955.
45. Ricci M.S., Jin Z., Dews M., Yu D., Thomas-Tikhonenko A., Dicker D.T., El-Deiry W.S. Direct repression of FLIP expression by c-myc is a major determinant of TRAIL sensitivity. Mol Cell Biol 2004, 24:8541-8555.
46. Zhang L., Ren X., Alt E., Bai X., Huang S., Xu Z., Lynch P.M., Moyer M.P., Wen X.F., Wu X. Chemoprevention of colorectal cancer by targeting APC-deficient cells for apoptosis. Nature 2010, 464:1058-1061.
47. Aza-Blanc P., Cooper C.L., Wagner K., Batalov S., Deveraux Q.L., Cooke M.P. Identification of modulators of TRAIL-induced apoptosis via RNAi-based phenotypic screening. Mol Cell 2003, 12:627-637.
48. Jin Z., Li Y., Pitti R., Lawrence D., Pham V.C., Lill J.R., Ashkenazi A. Cullin3-based polyubiquitination and p62-dependent aggregation of caspase-8 mediate extrinsic apoptosis signaling. Cell 2009, 137:721-735.
49. LeBlanc H., Lawrence D., Varfolomeev E., Totpal K., Morlan J., Schow P., Fong S., Schwall R., Sinicropi D., Ashkenazi A. Tumor-cell resistance to death receptor-induced apoptosis through mutational inactivation of the proapoptotic Bcl-2 homolog Bax. Nat Med 2002, 8:274-281.
50. Liu F.T., Agrawal S.G., Gribben J.G., Ye H., Du M.Q., Newland A.C., Jia L. Bortezomib blocks Bax degradation in malignant B cells during treatment with TRAIL. Blood 2008, 111:2797-2805.
51. Fulda S., Meyer E., Debatin K.M. Inhibition of TRAIL-induced apoptosis by Bcl-2 overexpression. Oncogene 2002, 21:2283-2294.
52. Hinz S., Trauzold A., Boenicke L., Sandberg C., Beckmann S., Bayer E., Walczak H., Kalthoff H., Ungefroren H. Bcl-XL protects pancreatic adenocarcinoma cells against CD95- and TRAIL-receptor-mediated apoptosis. Oncogene 2000, 19:5477-5486.
53. Kim S.H., Ricci M.S., El-Deiry W.S. Mcl-1: a gateway to TRAIL sensitization. Cancer Res 2008, 68:2062-2064.
54. Gillissen B., Wendt J., Richter A., Muer A., Overkamp T., Gebhardt N., Preissner R., Belka C., Dorken B., Daniel P.T. Endogenous Bak inhibitors Mcl-1 and Bcl-xL: differential impact on TRAIL resistance in Bax-deficient carcinoma. J Cell Biol 2010, 188:851-862.
55. Fesik S.W. Promoting apoptosis as a strategy for cancer drug discovery. Nat Rev Cancer 2005, 5:876-885.
56. LaCasse E.C., Mahoney D.J., Cheung H.H., Plenchette S., Baird S., Korneluk R.G. IAP-targeted therapies for cancer. Oncogene 2008, 27:6252-6275.
57. Cummins J.M., Kohli M., Rago C., Kinzler K.W., Vogelstein B., Bunz F. X-linked inhibitor of apoptosis protein (XIAP) is a nonredundant modulator of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-mediated apoptosis in human cancer cells. Cancer Res 2004, 64:3006-3008.
58. Vogler M., Walczak H., Stadel D., Haas T.L., Genze F., Jovanovic M., Gschwend J.E., Simmet T., Debatin K.M., Fulda S. Targeting XIAP bypasses Bcl-2-mediated resistance to TRAIL and cooperates with TRAIL to suppress pancreatic cancer growth in vitro and in vivo. Cancer Res 2008, 68:7956-7965.
59. Deng Y., Lin Y., Wu X. TRAIL-induced apoptosis requires Bax-dependent mitochondrial release of Smac/DIABLO. Genes Dev 2002, 16:33-45.
60. Li L., Thomas R.M., Suzuki H., De Brabander J.K., Wang X., Harran P.G. A small molecule Smac mimic potentiates TRAIL- and TNFalpha-mediated cell death. Science 2004, 305:1471-1474.
61. Vogler M., Walczak H., Stadel D., Haas T.L., Genze F., Jovanovic M., Bhanot U., Hasel C., Moller P., Gschwend J.E., et al. Small molecule XIAP inhibitors enhance TRAIL-induced apoptosis and antitumor activity in preclinical models of pancreatic carcinoma. Cancer Res 2009, 69:2425-2434.
62. Varfolomeev E., Alicke B., Elliott J.M., Zobel K., West K., Wong H., Scheer J.M., Ashkenazi A., Gould S.E., Fairbrother W.J., et al. X chromosome-linked inhibitor of apoptosis regulates cell death induction by proapoptotic receptor agonists. J Biol Chem 2009, 284:34553-34560.
63. Varfolomeev E., Maecker H., Sharp D., Lawrence D., Renz M., Vucic D., Ashkenazi A. Molecular determinants of kinase pathway activation by Apo2 ligand/tumor necrosis factor-related apoptosis-inducing ligand. J Biol Chem 2005, 280:40599-40608.
64. Falschlehner C., Emmerich C.H., Gerlach B., Walczak H. TRAIL signalling: decisions between life and death. Int J Biochem Cell Biol 2007, 39:1462-1475.
65. Karin M., Cao Y., Greten F.R., Li Z.W. NF-kappaB in cancer: from innocent bystander to major culprit. Nat Rev Cancer 2002, 2:301-310.
66. Braeuer S.J., Buneker C., Mohr A., Zwacka R.M. Constitutively activated nuclear factor-kappaB, but not induced NF-kappaB, leads to TRAIL resistance by up-regulation of X-linked inhibitor of apoptosis protein in human cancer cells. Mol Cancer Res 2006, 4:715-728.
67. Chen X., Kandasamy K., Srivastava R.K. Differential roles of RelA (p65) and c-Rel subunits of nuclear factor kappa B in tumor necrosis factor-related apoptosis-inducing ligand signaling. Cancer Res 2003, 63:1059-1066.
68. Brookd A.D., Jacobsten K.M., Li W., Shanker A., Sayers T.J. Bortezomib sensitizes human renal cell carcinomas to TRAIL apoptosis through increased activation of caspase-8 in the death-inducing signaling complex. Cancer Res 2010, 8:729-738.
69. Boehrer S., Nowak D., Puccetti E., Ruthardt M., Sattler N., Trepohl B., Schneider B., Hoelzer D., Mitrou P.S., Chow K.U. Prostate-apoptosis-response-gene-4 increases sensitivity to TRAIL-induced apoptosis. Leuk Res 2006, 30:597-605.
70. Burikhanov R., Zhao Y., Goswami A., Qiu S., Schwarze S.R., Rangnekar V.M. The tumor suppressor Par-4 activates an extrinsic pathway for apoptosis. Cell 2009, 138:377-388.