Is TRAIL the holy grail of cancer therapy?

Apoptosis

Volumn 14, Issue 4, 2009, Pages 607-623

  Newsom Davis, Thomas ^a   Prieske, Silvia ^a   Walczak, Henning ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Apoptosis; Cancer therapy; TRAIL; TRAIL resistance

Indexed keywords

1 [5 HYDROXY 2 (2 THIENYL) 4 QUINAZOLINYLAMINO] 3 METHYL 2,5 PYRROLEDIONE; ANTHRACYCLINE; APOMAB; BEVACIZUMAB; BMS 3455541; BORTEZOMIB; CARBOPLATIN; CETUXIMAB; CISPLATIN; DNA TOPOISOMERASE INHIBITOR; DOXORUBICIN; FLUOROURACIL; GEMCITABINE; IRINOTECAN; LEXATUMUMAB; LIGAND; MAPATUMUMAB; PACLITAXEL; PANITUMUMAB; PEMETREXED; PROTEASOME INHIBITOR; RITUXIMAB; SORAFENIB; TUMOR NECROSIS FACTOR RECEPTOR 2; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR; UNCLASSIFIED DRUG;

APOPTOSIS; CANCER CHEMOTHERAPY; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL TRIAL; COLORECTAL CANCER; DRUG EFFECT; FATIGUE; FEBRILE NEUTROPENIA; FEVER; HUMAN; HYPOTENSION; LUNG NON SMALL CELL CANCER; MONOTHERAPY; MULTIPLE MYELOMA; MYALGIA; NONHODGKIN LYMPHOMA; OVARY CANCER; PRIORITY JOURNAL; PROSTATE CANCER; REVIEW; THROMBOCYTOPENIA; TREATMENT DURATION;

APOPTOSIS; CELL SURVIVAL; CLINICAL TRIALS AS TOPIC; DRUG RESISTANCE, NEOPLASM; FORECASTING; HUMANS; MODELS, BIOLOGICAL; NEOPLASMS; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 62449166171     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-009-0321-2     Document Type: Review

References (163)

1. D Hanahan RA Weinberg 2000 The hallmarks of cancer Cell 100 57 70 10.1016/S0092-8674(00)81683-9
2. H Walczak RE Miller K Ariail 1999 Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo Nat Med 5 157 163 10.1038/5517
3. R Koschny H Holland J Sykora 2007 Bortezomib sensitizes primary human astrocytoma cells of WHO grades I to IV for tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis Clin Cancer Res 13 3403 3412 10.1158/1078-0432.CCR-07-0251
4. M Leverkus MR Sprick T Wachter 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 10.1128/MCB.23.3.777-790.2003
5. TM Ganten R Koschny TL Haas 2005 Proteasome inhibition sensitizes hepatocellular carcinoma cells, but not human hepatocytes, to TRAIL Hepatology 42 588 597 10.1002/hep.20807
6. RM Pitti SA Marsters S Ruppert CJ Donahue A Moore A Ashkenazi 1996 Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family J Biol Chem 271 12687 12690 10.1074/jbc.271.22.12687
7. SR Wiley K Schooley PJ Smolak 1995 Identification and characterization of a new member of the TNF family that induces apoptosis Immunity 3 673 682 10.1016/1074-7613(95)90057-8
8. G Pan J Ni YF Wei G Yu R Gentz VM Dixit 1997 An antagonist decoy receptor and a death domain-containing receptor for TRAIL Science 277 815 818 10.1126/science.277.5327.815
9. H Walczak MA Degli-Esposti RS Johnson 1997 TRAIL-R2: a novel apoptosis-mediating receptor for TRAIL EMBO J 16 5386 5397 10.1093/emboj/16.17. 5386
10. GR Screaton J Mongkolsapaya XN Xu AE Cowper AJ McMichael JI Bell 1997 TRICK2, a new alternatively spliced receptor that transduces the cytotoxic signal from TRAIL Curr Biol 7 693 696 10.1016/S0960-9822(06)00297-1
11. JP Sheridan SA Marsters RM Pitti 1997 Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors Science 277 818 821 10.1126/science.277.5327.818
12. GS Wu TF Burns ER McDonald 3rd 1997 KILLER/DR5 is a DNA damage-inducible p53-regulated death receptor gene Nat Genet 17 141 143 10.1038/ng1097-141
13. MA Degli-Esposti WC Dougall PJ Smolak JY Waugh CA Smith RG Goodwin 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 10.1016/S1074-7613(00)80399-4
14. MA Degli-Esposti PJ Smolak H Walczak 1997 Cloning and characterization of TRAIL-R3, a novel member of the emerging TRAIL receptor family J Exp Med 186 1165 1170 10.1084/jem.186.7.1165
15. A Lahm A Paradisi DR Green G Melino 2003 Death fold domain interaction in apoptosis Cell Death Differ 10 10 12 10.1038/sj.cdd.4401203
16. D Merino N Lalaoui A Morizot P Schneider E Solary O Micheau 2006 Differential inhibition of TRAIL-mediated DR5-DISC formation by decoy receptors 1 and 2 Mol Cell Biol 26 7046 7055 10.1128/MCB.00520-06
17. GS Wu TF Burns Y Zhan ES Alnemri WS El-Deiry 1999 Molecular cloning and functional analysis of the mouse homologue of the KILLER/DR5 tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) death receptor Cancer Res 59 2770 2775
18. P Schneider D Olson A Tardivel 2003 Identification of a new murine tumor necrosis factor receptor locus that contains two novel murine receptors for tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) J Biol Chem 278 5444 5454 10.1074/jbc.M210783200
19. S Vitovski JS Phillips J Sayers PI Croucher 2007 Investigating the interaction between osteoprotegerin and receptor activator of NF-kappaB or tumor necrosis factor-related apoptosis-inducing ligand: evidence for a pivotal role for osteoprotegerin in regulating two distinct pathways J Biol Chem 282 31601 31609 10.1074/jbc.M706078200
20. G Zauli E Rimondi V Nicolin E Melloni C Celeghini P Secchiero 2004 TNF-related apoptosis-inducing ligand (TRAIL) blocks osteoclastic differentiation induced by RANKL plus M-CSF Blood 104 2044 2050 10.1182/blood-2004-03-1196
21. E Cretney K Takeda H Yagita M Glaccum JJ Peschon MJ Smyth 2002 Increased susceptibility to tumor initiation and metastasis in TNF-related apoptosis-inducing ligand-deficient mice J Immunol 168 1356 1361
22. N Finnberg AJ Klein-Szanto WS El-Deiry 2008 TRAIL-R deficiency in mice promotes susceptibility to chronic inflammation and tumorigenesis J Clin Invest 118 111 123 10.1172/JCI29900
23. A Grosse-Wilde O Voloshanenko SL Bailey 2008 TRAIL-R deficiency in mice enhances lymph node metastasis without affecting primary tumor development J Clin Invest 118 100 110 10.1172/JCI33061
24. GE Diehl HH Yue K Hsieh 2004 TRAIL-R as a negative regulator of innate immune cell responses Immunity 21 877 889 10.1016/j.immuni.2004.11.008
25. H Ehrhardt S Fulda I Schmid J Hiscott KM Debatin I Jeremias 2003 TRAIL induced survival and proliferation in cancer cells resistant towards TRAIL-induced apoptosis mediated by NF-kappaB Oncogene 22 3842 3852 10.1038/sj.onc.1206520
26. N Ishimura H Isomoto SF Bronk GJ Gores 2006 Trail induces cell migration and invasion in apoptosis-resistant cholangiocarcinoma cells Am J Physiol Gastrointest Liver Physiol 290 G129 G136 10.1152/ajpgi.00242.2005
27. J Mongkolsapaya JM Grimes N Chen 1999 Structure of the TRAIL-DR5 complex reveals mechanisms conferring specificity in apoptotic initiation Nat Struct Biol 6 1048 1053 10.1038/14935
28. FC Kischkel S Hellbardt I Behrmann 1995 Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor EMBO J 14 5579 5588
29. MR Sprick MA Weigand E Rieser 2000 FADD/MORT1 and caspase-8 are recruited to TRAIL receptors 1 and 2 and are essential for apoptosis mediated by TRAIL receptor 2 Immunity 12 599 609 10.1016/S1074-7613(00)80211-3
30. FC Kischkel DA Lawrence A Chuntharapai P Schow KJ Kim A Ashkenazi 2000 Apo2L/TRAIL-dependent recruitment of endogenous FADD and caspase-8 to death receptors 4 and 5 Immunity 12 611 620 10.1016/S1074-7613(00)80212-5
31. FC Kischkel DA Lawrence A Tinel 2001 Death receptor recruitment of endogenous caspase-10 and apoptosis initiation in the absence of caspase-8 J Biol Chem 276 46639 46646 10.1074/jbc.M105102200
32. MR Sprick E Rieser H Stahl A Grosse-Wilde MA Weigand H Walczak 2002 Caspase-10 is recruited to and activated at the native TRAIL and CD95 death-inducing signalling complexes in a FADD-dependent manner but can not functionally substitute caspase-8 EMBO J 21 4520 4530 10.1093/emboj/cdf441
33. A Krueger I Schmitz S Baumann PH Krammer S Kirchhoff 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 10.1074/jbc.M101780200
34. A Golks D Brenner C Fritsch PH Krammer IN Lavrik 2005 c-FLIPR, a new regulator of death receptor-induced apoptosis J Biol Chem 280 14507 14513 10.1074/jbc.M414425200
35. M Thome P Schneider K Hofmann 1997 Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors Nature 386 517 521 10.1038/386517a0
36. M Irmler M Thome M Hahne 1997 Inhibition of death receptor signals by cellular FLIP Nature 388 190 195 10.1038/40657
37. O Micheau M Thome P Schneider 2002 The long form of FLIP is an activator of caspase-8 at the Fas death-inducing signaling complex J Biol Chem 277 45162 45171 10.1074/jbc.M206882200
38. EE Varfolomeev M Schuchmann V Luria 1998 Targeted disruption of the mouse Caspase 8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally Immunity 9 267 276 10.1016/S1074-7613(00)80609-3
39. J Zhang D Cado A Chen NH Kabra A Winoto 1998 Fas-mediated apoptosis and activation-induced T-cell proliferation are defective in mice lacking FADD/Mort1 Nature 392 296 300 10.1038/32681
40. HR Stennicke JM Jurgensmeier H Shin 1998 Pro-caspase-3 is a major physiologic target of caspase-8 J Biol Chem 273 27084 27090 10.1074/jbc.273.42. 27084
41. BC Barnhart EC Alappat ME Peter 2003 The CD95 type I/type II model Semin Immunol 15 185 193 10.1016/S1044-5323(03)00031-9
42. NJ Waterhouse JE Ricci DR Green 2002 And all of a sudden it's over: mitochondrial outer-membrane permeabilization in apoptosis Biochimie 84 113 121 10.1016/S0300-9084(02)01379-2
43. XM Yin 2006 Bid, a BH3-only multi-functional molecule, is at the cross road of life and death Gene 369 7 19 10.1016/j.gene.2005.10.038
44. R Koschny H Walczak TM Ganten 2007 The promise of TRAIL-potential and risks of a novel anticancer therapy J Mol Med 85 923 935 10.1007/s00109-007- 0194-1
45. HN LeBlanc A Ashkenazi 2003 Apo2L/TRAIL and its death and decoy receptors Cell Death Differ 10 66 75 10.1038/sj.cdd.4401187
46. FC Kimberley GR Screaton 2004 Following a TRAIL: update on a ligand and its five receptors Cell Res 14 359 372 10.1038/sj.cr.7290236
47. MS Sheikh Y Huang EA Fernandez-Salas 1999 The antiapoptotic decoy receptor TRID/TRAIL-R3 is a p53-regulated DNA damage-inducible gene that is overexpressed in primary tumors of the gastrointestinal tract Oncogene 18 4153 4159 10.1038/sj.onc.1202763
48. M Hornstein MJ Hoffmann A Alexa 2008 Protein phosphatase and TRAIL receptor genes as new candidate tumor genes on chromosome 8p in prostate cancer Cancer Genomics Proteomics 5 123 136
49. P Horak D Pils G Haller 2005 Contribution of epigenetic silencing of tumor necrosis factor-related apoptosis inducing ligand receptor 1 (DR4) to TRAIL resistance and ovarian cancer Mol Cancer Res 3 335 343 10.1158/1541-7786.MCR-04-0136
50. E Saulle A Petronelli L Pasquini 2007 Proteasome inhibitors sensitize ovarian cancer cells to TRAIL induced apoptosis Apoptosis 12 635 655 10.1007/s10495-006-0025-9
51. LB Pritzker M Scatena CM Giachelli 2004 The role of osteoprotegerin and tumor necrosis factor-related apoptosis-inducing ligand in human microvascular endothelial cell survival Mol Biol Cell 15 2834 2841 10.1091/mbc.E04-01-0059
52. EN De Toni SE Thieme A Herbst 2008 OPG is regulated by beta-catenin and mediates resistance to TRAIL-induced apoptosis in colon cancer Clin Cancer Res 14 4713 4718 10.1158/1078-0432.CCR-07-5019
53. P Horak D Pils A Kaider 2005 Perturbation of the tumor necrosis factor-related apoptosis-inducing ligand cascade in ovarian cancer: overexpression of FLIPL and deregulation of the functional receptors DR4 and DR5 Clin Cancer Res 11 8585 8591 10.1158/1078-0432.CCR-05-1276
54. P Clarke KL Tyler 2007 Down-regulation of cFLIP following reovirus infection sensitizes human ovarian cancer cells to TRAIL-induced apoptosis Apoptosis 12 211 223 10.1007/s10495-006-0528-4
55. P Geserick C Drewniok M Hupe 2008 Suppression of cFLIP is sufficient to sensitize human melanoma cells to TRAIL- and CD95L-mediated apoptosis Oncogene 27 3211 3220 10.1038/sj.onc.1210985
56. D Siegmund P Hadwiger K Pfizenmaier HP Vornlocher H Wajant 2002 Selective inhibition of FLICE-like inhibitory protein expression with small interfering RNA oligonucleotides is sufficient to sensitize tumor cells for TRAIL-induced apoptosis Mol Med 8 725 732
57. TM Ganten TL Haas J Sykora 2004 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 Differ 11 Suppl 1 S86 S96 10.1038/sj.cdd.4401437
58. S Hopkins-Donaldson JL Bodmer KB Bourloud CB Brognara J Tschopp N Gross 2000 Loss of caspase-8 expression in highly malignant human neuroblastoma cells correlates with resistance to tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis Cancer Res 60 4315 4319
59. P Makhov K Golovine RG Uzzo 2008 Zinc chelation induces rapid depletion of the X-linked inhibitor of apoptosis and sensitizes prostate cancer cells to TRAIL-mediated apoptosis Cell Death Differ 15 1745 1751 10.1038/cdd.2008.106
60. Y Huang M Lu H Wu 2004 Antagonizing XIAP-mediated caspase-3 inhibition. Achilles' heel of cancers? Cancer Cell 5 1 2 10.1016/S1535-6108(03)00340-4
61. O Micheau D Merino 2004 Controlling TRAIL-mediated caspase-3 activation Leukemia 18 1578 1580 10.1038/sj.leu.2403497
62. Y Shi 2004 Caspase activation, inhibition, and reactivation: a mechanistic view Protein Sci 13 1979 1987 10.1110/ps.04789804
63. S Hinz A Trauzold L Boenicke 2000 Bcl-XL protects pancreatic adenocarcinoma cells against CD95- and TRAIL-receptor-mediated apoptosis Oncogene 19 5477 5486 10.1038/sj.onc.1203936
64. S Fulda E Meyer KM Debatin 2002 Inhibition of TRAIL-induced apoptosis by Bcl-2 overexpression Oncogene 21 2283 2294 10.1038/sj.onc.1205258
65. JM Adams S Cory 2007 The Bcl-2 apoptotic switch in cancer development and therapy Oncogene 26 1324 1337 10.1038/sj.onc.1210220
66. M Taniai A Grambihler H Higuchi 2004 Mcl-1 mediates tumor necrosis factor-related apoptosis-inducing ligand resistance in human cholangiocarcinoma cells Cancer Res 64 3517 3524 10.1158/0008-5472.CAN-03-2770
67. O Ndozangue-Touriguine M Sebbagh D Merino O Micheau J Bertoglio J Breard 2008 A mitochondrial block and expression of XIAP lead to resistance to TRAIL-induced apoptosis during progression to metastasis of a colon carcinoma Oncogene 27 6012 6022 10.1038/onc.2008.197
68. M Vogler H Walczak D Stadel 2008 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 68 7956 7965 10.1158/0008-5472.CAN-08- 1296
69. H Wajant 2004 TRAIL and NFkappaB signaling-a complex relationship Vitam Horm 67 101 132 10.1016/S0083-6729(04)67007-5
70. H Li X Lin 2008 Positive and negative signaling components involved in TNFalpha-induced NF-kappaB activation Cytokine 41 1 8 10.1016/j.cyto.2007.09.016
71. N Harper SN Farrow A Kaptein GM Cohen M MacFarlane 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 10.1074/jbc. M105693200
72. E Varfolomeev H Maecker D Sharp 2005 Molecular determinants of kinase pathway activation by Apo2 ligand/tumor necrosis factor-related apoptosis-inducing ligand J Biol Chem 280 40599 40608 10.1074/jbc.M509560200
73. P Secchiero C Zerbinati E Rimondi 2004 TRAIL promotes the survival, migration and proliferation of vascular smooth muscle cells Cell Mol Life Sci 61 1965 1974 10.1007/s00018-004-4197-6
74. P Secchiero E Melloni F Corallini 2008 TRAIL promotes migration of human bone marrow multipotent stromal cells Stem Cells 26 11 2955 2963
75. U Vilimanovich V Bumbasirevic 2008 TRAIL induces proliferation of human glioma cells by c-FLIPL-mediated activation of ERK1/2 Cell Mol Life Sci 65 814 826 10.1007/s00018-008-7513-8
76. LL Belyanskaya A Ziogas S Hopkins-Donaldson 2008 TRAIL-induced survival and proliferation of SCLC cells is mediated by ERK and dependent on TRAIL-R2/DR5 expression in the absence of caspase-8 Lung Cancer 60 355 365 10.1016/j.lungcan.2007.11.005
77. P Secchiero A Gonelli E Carnevale 2003 TRAIL promotes the survival and proliferation of primary human vascular endothelial cells by activating the Akt and ERK pathways Circulation 107 2250 2256 10.1161/01.CIR.0000062702.60708.C4
78. AM Joy CE Beaudry NL Tran 2003 Migrating glioma cells activate the PI3-K pathway and display decreased susceptibility to apoptosis J Cell Sci 116 4409 4417 10.1242/jcs.00712
79. A Trauzold D Siegmund B Schniewind 2006 TRAIL promotes metastasis of human pancreatic ductal adenocarcinoma Oncogene 25 7434 7439 10.1038/sj.onc.1209719
80. AD Sanlioglu AF Korcum E Pestereli 2007 TRAIL death receptor-4 expression positively correlates with the tumor grade in breast cancer patients with invasive ductal carcinoma Int J Radiat Oncol Biol Phys 69 716 723 10.1016/j.ijrobp.2007.03.057
81. P Schneider 2000 Production of recombinant TRAIL and TRAIL receptor: Fc chimeric proteins Methods Enzymol 322 325 345 10.1016/S0076-6879(00)22031-4
82. TM Ganten R Koschny J Sykora 2006 Preclinical differentiation between apparently safe and potentially hepatotoxic applications of TRAIL either alone or in combination with chemotherapeutic drugs Clin Cancer Res 12 2640 2646 10.1158/1078-0432.CCR-05-2635
83. GJ Gores SH Kaufmann 2001 Is TRAIL hepatotoxic? Hepatology 34 3 6 10.1053/jhep.2001.25173a
84. D Lawrence Z Shahrokh S Marsters 2001 Differential hepatocyte toxicity of recombinant Apo2L/TRAIL versions Nat Med 7 383 385 10.1038/86397
85. A Ashkenazi RC Pai S Fong 1999 Safety and antitumor activity of recombinant soluble Apo2 ligand J Clin Invest 104 155 162 10.1172/JCI6926
86. SK Kelley A Ashkenazi 2004 Targeting death receptors in cancer with Apo2L/TRAIL Curr Opin Pharmacol 4 333 339 10.1016/j.coph.2004.02.006
87. DJ Buchsbaum T Zhou AF Lobuglio 2006 TRAIL receptor-targeted therapy Future Oncol 2 493 508 10.2217/14796694.2.4.493
88. A Natoni M MacFarlane S Inoue 2007 TRAIL signals to apoptosis in chronic lymphocytic leukaemia cells primarily through TRAIL-R1 whereas cross-linked agonistic TRAIL-R2 antibodies facilitate signalling via TRAIL-R2 Br J Haematol 139 568 577 10.1111/j.1365-2141.2007.06852.x
89. A Chuntharapai K Dodge K Grimmer 2001 Isotype-dependent inhibition of tumor growth in vivo by monoclonal antibodies to death receptor 4 J Immunol 166 4891 4898
90. DJ Buchsbaum T Zhou WE Grizzle 2003 Antitumor efficacy of TRA-8 anti-DR5 monoclonal antibody alone or in combination with chemotherapy and/or radiation therapy in a human breast cancer model Clin Cancer Res 9 3731 3741
91. K Ichikawa W Liu L Zhao 2001 Tumoricidal activity of a novel anti-human DR5 monoclonal antibody without hepatocyte cytotoxicity Nat Med 7 954 960 10.1038/91000
92. Y Zeng XX Wu M Fiscella 2006 Monoclonal antibody to tumor necrosis factor-related apoptosis-inducing ligand receptor 2 (TRAIL-R2) induces apoptosis in primary renal cell carcinoma cells in vitro and inhibits tumor growth in vivo Int J Oncol 28 421 430
93. M MacFarlane S Inoue SL Kohlhaas 2005 Chronic lymphocytic leukemic cells exhibit apoptotic signaling via TRAIL-R1 Cell Death Differ 12 773 782 10.1038/sj.cdd.4401649
94. K Takeda N Yamaguchi H Akiba 2004 Induction of tumor-specific T cell immunity by anti-DR5 antibody therapy J Exp Med 199 437 448 10.1084/jem.20031457
95. L Pukac P Kanakaraj R Humphreys 2005 HGS-ETR1, a fully human TRAIL-receptor 1 monoclonal antibody, induces cell death in multiple tumour types in vitro and in vivo Br J Cancer 92 1430 1441 10.1038/sj.bjc.6602487
96. Y Gazitt 1999 TRAIL is a potent inducer of apoptosis in myeloma cells derived from multiple myeloma patients and is not cytotoxic to hematopoietic stem cells Leukemia 13 1817 1824 10.1038/sj/leu/2401501
97. CS Mitsiades SP Treon N Mitsiades 2001 TRAIL/Apo2L ligand selectively induces apoptosis and overcomes drug resistance in multiple myeloma: therapeutic applications Blood 98 795 804 10.1182/blood.V98.3.795
98. K Clodi D Wimmer Y Li 2000 Expression of tumour necrosis factor (TNF)-related apoptosis-inducing ligand (TRAIL) receptors and sensitivity to TRAIL-induced apoptosis in primary B-cell acute lymphoblastic leukaemia cells Br J Haematol 111 580 586 10.1046/j.1365-2141.2000.02404.x
99. M MacFarlane N Harper RT Snowden 2002 Mechanisms of resistance to TRAIL-induced apoptosis in primary B cell chronic lymphocytic leukaemia Oncogene 21 6809 6818 10.1038/sj.onc.1205853
100. V Snell K Clodi S Zhao 1997 Activity of TNF-related apoptosis-inducing ligand (TRAIL) in haematological malignancies Br J Haematol 99 618 624 10.1046/j.1365-2141.1997.4393250.x
101. M Clayer S Bouralexis A Evdokiou S Hay GJ Atkins DM Findlay 2001 Enhanced apoptosis of soft tissue sarcoma cells with chemotherapy: a potential new approach using TRAIL J Orthop Surg (Hong Kong) 9 19 22
102. A Panner CD James MS Berger RO Pieper 2005 mTOR controls FLIPS translation and TRAIL sensitivity in glioblastoma multiforme cells Mol Cell Biol 25 8809 8823 10.1128/MCB.25.20.8809-8823.2005
103. M Todaro Y Lombardo MG Francipane 2008 Apoptosis resistance in epithelial tumors is mediated by tumor-cell-derived interleukin-4 Cell Death Differ 15 762 772 10.1038/sj.cdd.4402305
104. A Younes JM Vose AD Zelenetz 2005 Results of a phase 2 trial of HGS-ETR1 (agonistic human monoclonal antibody to TRAIL receptor 1) in subjects with relapsed/refractory Non-Hodgkin's Lymphoma (NHL) Blood 106 489 ASH Annual Meeting Abstracts
105. AW Tolcher M Mita NJ Meropol 2007 Phase I pharmacokinetic and biologic correlative study of mapatumumab, a fully human monoclonal antibody with agonist activity to tumor necrosis factor-related apoptosis-inducing ligand receptor-1 J Clin Oncol 25 1390 1395 10.1200/JCO.2006.08.8898
106. SJ Hotte HW Hirte EX Chen 2008 A phase 1 study of mapatumumab (fully human monoclonal antibody to TRAIL-R1) in patients with advanced solid malignancies Clin Cancer Res 14 3450 3455 10.1158/1078-0432.CCR-07-1416
107. LH Le HW Hirte SJ Hotte 2004 Phase I study of a fully human monoclonal antibody to the tumor necrosis factor-related apoptosis-inducing ligand death receptor 4 (TRAIL-R1) in subjects with advanced solid malignancies or non-Hodgkin's lymphoma (NHL) J Clin Oncol 22 2533 Meeting Abstracts
108. FA Greco P Bonomi J Crawford 2008 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 61 82 90 10.1016/j.lungcan.2007.12.011
109. R Plummer G Attard S Pacey 2007 Phase 1 and pharmacokinetic study of lexatumumab in patients with advanced cancers Clin Cancer Res 13 6187 6194 10.1158/1078-0432.CCR-07-0950
110. A Patnaik H Wakelee M Mita 2006 HGS-ETR2-A fully human monoclonal antibody to TRAIL-R2: results of a phase I trial in patients with advanced solid tumors J Clin Oncol 24 3012 ASCO Meeting Abstracts
111. D Camidge RS Herbst M Gordon 2007 A phase I safety and pharmacokinetic study of apomab, a human DR5 agonist antibody, in patients with advanced cancer J Clin Oncol 25 3582 ASCO Meeting Abstracts
112. P LoRusso D Hong E Heath 2007 First-in-human study of AMG 655, a pro-apoptotic TRAIL receptor-2 agonist, in adult patients with advanced solid tumors J Clin Oncol 25 3534 ASCO Meeting Abstracts
113. RS Herbst DS Mendolson S Ebbinghaus 2006 A phase I safety and pharmacokinetic (PK) study of recombinant Apo2L/TRAIL, an apoptosis-inducing protein in patients with advanced cancer J Clin Oncol 24 3013 10.1200/JCO.2005.04.8678 Meeting Abstracts
114. A Yada M Yazawa S Ishida 2008 A novel humanized anti-human death receptor 5 antibody CS-1008 induces apoptosis in tumor cells without toxicity in hepatocytes Ann Oncol 19 1060 1067 10.1093/annonc/mdn015
115. G Jonsson S Paulie A Grandien 2003 High level of cFLIP correlates with resistance to death receptor-induced apoptosis in bladder carcinoma cells Anticancer Res 23 1213 1218
116. MM McCarthy M Sznol KA DiVito RL Camp DL Rimm HM Kluger 2005 Evaluating the expression and prognostic value of TRAIL-R1 and TRAIL-R2 in breast cancer Clin Cancer Res 11 5188 5194 10.1158/1078-0432.CCR-05-0158
117. J Strater U Hinz H Walczak 2002 Expression of TRAIL and TRAIL receptors in colon carcinoma: TRAIL-R1 is an independent prognostic parameter Clin Cancer Res 8 3734 3740
118. Y Pan R Xu M Peach 2007 Application of pharmacodynamic assays in a phase Ia trial of Apo2L/TRAIL in patients with advanced tumors J Clin Oncol 25 3535 ASCO Meeting Abstracts
119. R Koschny TM Ganten J Sykora 2007 TRAIL/bortezomib cotreatment is potentially hepatotoxic but induces cancer-specific apoptosis within a therapeutic window Hepatology 45 649 658 10.1002/hep.21555
120. A El-Zawahry J McKillop C Voelkel-Johnson 2005 Doxorubicin increases the effectiveness of Apo2L/TRAIL for tumor growth inhibition of prostate cancer xenografts BMC Cancer 5 2 10.1186/1471-2407-5-2
121. S Shankar TR Singh RK Srivastava 2004 Ionizing radiation enhances the therapeutic potential of TRAIL in prostate cancer in vitro and in vivo: intracellular mechanisms Prostate 61 35 49 10.1002/pros.20069
122. S Shankar X Chen RK Srivastava 2005 Effects of sequential treatments with chemotherapeutic drugs followed by TRAIL on prostate cancer in vitro and in vivo Prostate 62 165 186 10.1002/pros.20126
123. S Shamimi-Noori WS Yeow MF Ziauddin 2008 Cisplatin enhances the antitumor effect of tumor necrosis factor-related apoptosis-inducing ligand gene therapy via recruitment of the mitochondria-dependent death signaling pathway Cancer Gene Ther 15 356 370 10.1038/sj.cgt.7701120
124. S Ray A Almasan 2003 Apoptosis induction in prostate cancer cells and xenografts by combined treatment with Apo2 ligand/tumor necrosis factor-related apoptosis-inducing ligand and CPT-11 Cancer Res 63 4713 4723
125. LQ Chow SG Eckhardt DL Gustafson 2006 HGS-ETR1, an antibody targeting TRAIL-R1, in combination with paclitaxel and carboplatin in patients with advanced solid malignancies: results of a phase 1 and PK study J Clin Oncol 24 2515 ASCO Meeting Abstracts
126. C Oldenhuis C Mom S Sleijfer 2008 A phase I study with the agonistic TRAIL-R1 antibody, mapatumumab, in combination with gemcitabine and cisplatin J Clin Oncol 26 3540 ASCO Meeting Abstracts
127. BI Sikic HA Wakelee M von Mehren 2007 A phase Ib study to assess the safety of lexatumumab, a human monoclonal antibody that activates TRAIL-R2, in combination with gemcitabine, pemetrexed, doxorubicin or FOLFIRI J Clin Oncol 25 14006 ASCO Meeting Abstracts
128. J Held K Schulze-Osthoff 2001 Potential and caveats of TRAIL in cancer therapy Drug Resist Updat 4 243 252 10.1054/drup.2001.0208
129. N Mitsiades CS Mitsiades V Poulaki 2002 Biologic sequelae of nuclear factor-kappaB blockade in multiple myeloma: therapeutic applications Blood 99 4079 4086 10.1182/blood.V99.11.4079
130. D Daniel B Yang DA Lawrence 2007 Cooperation of the proapoptotic receptor agonist rhApo2L/TRAIL with the CD20 antibody rituximab against non-Hodgkin lymphoma xenografts Blood 110 4037 4046 10.1182/blood-2007-02-076075
131. L Yee M Fanale K Dimick 2007 A phase IB safety and pharmacokinetic (PK) study of recombinant human Apo2L/TRAIL in combination with rituximab in patients with low-grade non-Hodgkin lymphoma J Clin Oncol 25 8078 ASCO Meeting Abstracts
132. TJ Sayers AD Brooks CY Koh 2003 The proteasome inhibitor PS-341 sensitizes neoplastic cells to TRAIL-mediated apoptosis by reducing levels of c-FLIP Blood 102 303 310 10.1182/blood-2002-09-2975
133. WH Hallett E Ames M Motarjemi 2008 Sensitization of tumor cells to NK cell-mediated killing by proteasome inhibition J Immunol 180 163 170
134. A Shanker AD Brooks CA Tristan 2008 Treating metastatic solid tumors with bortezomib and a tumor necrosis factor-related apoptosis-inducing ligand receptor agonist antibody J Natl Cancer Inst 100 649 662 10.1093/jnci/djn113
135. F Guo C Sigua J Tao 2004 Cotreatment with histone deacetylase inhibitor LAQ824 enhances Apo-2L/tumor necrosis factor-related apoptosis inducing ligand-induced death inducing signaling complex activity and apoptosis of human acute leukemia cells Cancer Res 64 2580 2589 10.1158/0008-5472.CAN-03-2629
136. RR Rosato JA Almenara Y Dai S Grant 2003 Simultaneous activation of the intrinsic and extrinsic pathways by histone deacetylase (HDAC) inhibitors and tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) synergistically induces mitochondrial damage and apoptosis in human leukemia cells Mol Cancer Ther 2 1273 1284
137. S Inoue M MacFarlane N Harper LM Wheat MJ Dyer GM Cohen 2004 Histone deacetylase inhibitors potentiate TNF-related apoptosis-inducing ligand (TRAIL)-induced apoptosis in lymphoid malignancies Cell Death Differ 11 Suppl 2 S193 S206 10.1038/sj.cdd.4401535
138. A Nebbioso N Clarke E Voltz 2005 Tumor-selective action of HDAC inhibitors involves TRAIL induction in acute myeloid leukemia cells Nat Med 11 77 84 10.1038/nm1161
139. A Pathil S Armeanu S Venturelli 2006 HDAC inhibitor treatment of hepatoma cells induces both TRAIL-independent apoptosis and restoration of sensitivity to TRAIL Hepatology 43 425 434 10.1002/hep.21054
140. X Volkmann U Fischer MJ Bahr 2007 Increased hepatotoxicity of tumor necrosis factor-related apoptosis-inducing ligand in diseased human liver Hepatology 46 1498 1508 10.1002/hep.21846
141. AJ Frew RK Lindemann BP Martin 2008 Combination therapy of established cancer using a histone deacetylase inhibitor and a TRAIL receptor agonist Proc Natl Acad Sci USA 105 11317 11322 10.1073/pnas.0801868105
142. H Wu J Tschopp SC Lin 2007 Smac mimetics and TNFalpha: a dangerous liaison? Cell 131 655 658 10.1016/j.cell.2007.10.042
143. SL Petersen L Wang A Yalcin-Chin 2007 Autocrine TNFalpha signaling renders human cancer cells susceptible to Smac-mimetic-induced apoptosis Cancer Cell 12 445 456 10.1016/j.ccr.2007.08.029
144. JE Vince WW Wong N Khan 2007 IAP antagonists target cIAP1 to induce TNFalpha-dependent apoptosis Cell 131 682 693 10.1016/j.cell.2007.10.037
145. E Varfolomeev JW Blankenship SM Wayson 2007 IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis Cell 131 669 681 10.1016/j.cell.2007.10.030
146. L Li RM Thomas H Suzuki JK De Brabander X Wang PG Harran 2004 A small molecule Smac mimic potentiates TRAIL- and TNFalpha-mediated cell death Science 305 1471 1474 10.1126/science.1098231
147. E Petrucci L Pasquini A Petronelli 2007 A small molecule Smac mimic potentiates TRAIL-mediated cell death of ovarian cancer cells Gynecol Oncol 105 481 492 10.1016/j.ygyno.2007.01.011
148. M Shrader MS Pino L Lashinger 2007 Gefitinib reverses TRAIL resistance in human bladder cancer cell lines via inhibition of AKT-mediated X-linked inhibitor of apoptosis protein expression Cancer Res 67 1430 1435 10.1158/0008-5472.CAN-06-1224
149. C Garcia-Echeverria WR Sellers 2008 Drug discovery approaches targeting the PI3K/Akt pathway in cancer Oncogene 27 5511 5526 10.1038/onc.2008.246
150. E Bremer J Kuijlen D Samplonius H Walczak L de Leij W Helfrich 2004 Target cell-restricted and -enhanced apoptosis induction by a scFv:sTRAIL fusion protein with specificity for the pancarcinoma-associated antigen EGP2 Int J Cancer 109 281 290 10.1002/ijc.11702
151. E Bremer D Samplonius BJ Kroesen L van Genne L de Leij W Helfrich 2004 Exceptionally potent anti-tumor bystander activity of an scFv:sTRAIL fusion protein with specificity for EGP2 toward target antigen-negative tumor cells Neoplasia 6 636 645 10.1593/neo.04229
152. E Bremer DF Samplonius M Peipp 2005 Target cell-restricted apoptosis induction of acute leukemic T cells by a recombinant tumor necrosis factor-related apoptosis-inducing ligand fusion protein with specificity for human CD7 Cancer Res 65 3380 3388
153. J Stieglmaier E Bremer C Kellner 2008 Selective induction of apoptosis in leukemic B-lymphoid cells by a CD19-specific TRAIL fusion protein Cancer Immunol Immunother 57 233 246 10.1007/s00262-007-0370-8
154. E Bremer DF Samplonius L van Genne 2005 Simultaneous inhibition of epidermal growth factor receptor (EGFR) signaling and enhanced activation of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) receptor-mediated apoptosis induction by an scFv:sTRAIL fusion protein with specificity for human EGFR J Biol Chem 280 10025 10033 10.1074/jbc.M413673200
155. TS Griffith EL Broghammer 2001 Suppression of tumor growth following intralesional therapy with TRAIL recombinant adenovirus Mol Ther 4 257 266 10.1006/mthe.2001.0439
156. JR Herman HL Adler E Aguilar-Cordova 1999 In situ gene therapy for adenocarcinoma of the prostate: a phase I clinical trial Hum Gene Ther 10 1239 1249 10.1089/10430349950018229
157. R Ravi GC Bedi LW Engstrom 2001 Regulation of death receptor expression and TRAIL/Apo2L-induced apoptosis by NF-kappaB Nat Cell Biol 3 409 416 10.1038/35070096
158. M Romagnoli G Desplanques S Maiga 2007 Canonical nuclear factor kappaB
159. G Roue P Perez-Galan M Lopez-Guerra N Villamor E Campo D Colomer 2007 Selective inhibition of IkappaB kinase sensitizes mantle cell lymphoma B cells to TRAIL by decreasing cellular FLIP level J Immunol 178 1923 1930
160. KM Kim JJ Song JY An YT Kwon YJ Lee 2005 Pretreatment of acetylsalicylic acid promotes tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis by down-regulating BCL-2 gene expression J Biol Chem 280 41047 41056 10.1074/jbc.M503713200
161. T Uno K Takeda Y Kojima 2006 Eradication of established tumors in mice by a combination antibody-based therapy Nat Med 12 693 698 10.1038/nm1405
162. K Takeda Y Kojima K Ikejima 2008 Death receptor 5 mediated-apoptosis contributes to cholestatic liver disease Proc Natl Acad Sci USA 105 10895 10900 10.1073/pnas.0802702105
163. G Suntharalingam MR Perry S Ward 2006 Cytokine storm in a phase 1 trial of the anti-CD28 monoclonal antibody TGN1412 N Engl J Med 355 1018 1028 10.1056/NEJMoa063842