TRAIL signaling and synergy mechanisms used in TRAIL-based combination therapies

Molecular Cancer Therapeutics

Volumn 11, Issue 1, 2012, Pages 3-13

  Hellwig, Christian T ^a,b   Rehm, Markus ^b  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; BEVACIZUMAB; BORTEZOMIB; CAMPTOTHECIN; CAPECITABINE; CARBOPLATIN; CETUXIMAB; CISPLATIN; CONATUMUMAB; DOXORUBICIN; DROZITUMAB; DULANERMIN; FAS LIGAND; FLUOROURACIL; GEMCITABINE; HISTONE DEACETYLASE INHIBITOR; IRINOTECAN; ISOSORBIDE; LEXATUMUMAB; MAPATUMUMAB; NAVITOCLAX; OBATOCLAX; PACLITAXEL; PHOSPHOTRANSFERASE INHIBITOR; PROTEASOME INHIBITOR; RECOMBINANT TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TIGATUZUMAB; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNINDEXED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BREAST CANCER; CANCER COMBINATION CHEMOTHERAPY; CANCER RADIOTHERAPY; CANCER SURVIVAL; COLORECTAL CANCER; DRUG EFFICACY; DRUG HALF LIFE; DRUG POTENTIATION; DRUG TOLERABILITY; HUMAN; LIVER TOXICITY; LUNG NON SMALL CELL CANCER; LYMPHOMA; MONOTHERAPY; MULTIPLE MYELOMA; NONHODGKIN LYMPHOMA; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; SOFT TISSUE SARCOMA; SOLID TUMOR; TREATMENT RESPONSE; UNSPECIFIED SIDE EFFECT; UTERINE CERVIX CANCER;

ANTIBODIES; ANTINEOPLASTIC AGENTS; APOPTOSIS; CLINICAL TRIALS AS TOPIC; DRUG THERAPY, COMBINATION; HUMANS; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; SIGNAL TRANSDUCTION; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84855643244     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-11-0434     Document Type: Review

References (75)

1. Costelli P, Aoki P, Zingaro B, Carbó N, Reffo P, Lopez-Soriano FJ, et al. Mice lacking TNFalpha receptors 1 and 2 are resistant to death and fulminant liver injury induced by agonistic anti-Fas antibody. Cell Death Differ 2003;10:997-1004. (Pubitemid 37069477)
2. Ogasawara J, Watanabe-Fukunaga R, Adachi M, Matsuzawa A, Kasugai T, Kitamura Y, et al. Lethal effect of the anti-Fas antibody in mice. Nature 1993;364:806-9. (Pubitemid 23261761)
3. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, Kubin M, et al. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 1999;5:157-63. (Pubitemid 29068521)
4. Ashkenazi A, Pai RC, Fong S, Leung S, Lawrence DA, Marsters SA, et al. Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest 1999;104:155-62.
5. Wiley SR, Schooley K, Smolak PJ, Din WS, Huang CP, Nicholl JK, et al. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 1995;3:673-82. (Pubitemid 26091143)
6. Pitti RM, Marsters SA, Ruppert S, Donahue CJ, Moore A, Ashkenazi A. Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J Biol Chem 1996;271:12687-90. (Pubitemid 26175834)
7. Smyth MJ, Cretney E, Takeda K, Wiltrout RH, Sedger LM, Kayagaki N, et al. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) contributes to interferon gamma-dependent natural killer cell protection from tumor metastasis. J Exp Med 2001;193:661-70. (Pubitemid 32524460)
8. Cretney E, Takeda K, Yagita H, Glaccum M, Peschon JJ, Smyth MJ. Increased susceptibility to tumor initiation and metastasis in TNF-related apoptosis-inducing ligand-deficient mice. J Immunol 2002;168:1356-61. (Pubitemid 34094506)
9. Janssen EM, Droin NM,Lemmens EE, Pinkoski MJ, Bensinger SJ, Ehst BD, et al. CD4+ T-cell help controls CD8+ T-cell memory via TRAIL-mediated activation-induced cell death. Nature 2005;434:88-93. (Pubitemid 40349390)
10. Zhang XR, Zhang LY, Devadas S, Li L, Keegan AD, Shi YF. Reciprocal expression of TRAIL and CD95L in Th1 and Th2 cells: role of apoptosis in T helper subset differentiation. Cell Death Differ 2003;10:203-10. (Pubitemid 36553462)
11. MacFarlane M, Ahmad M, Srinivasula SM, Fernandes-Alnemri T, Cohen GM, Alnemri ES. Identification and molecular cloning of two novel receptors for the cytotoxic ligand TRAIL. J Biol Chem 1997;272:25417-20. (Pubitemid 27438841)
12. Pan G, O'Rourke K, Chinnaiyan AM, Gentz R, Ebner R, Ni J, et al. The receptor for the cytotoxic ligand TRAIL. Science 1997;276:111-3. (Pubitemid 27161256)
13. Walczak H, Degli-Esposti MA, Johnson RS, Smolak PJ, Waugh JY, Boiani N, et al. TRAIL-R2: a novel apoptosis-mediating receptor for TRAIL. EMBO J 1997;16:5386-97. (Pubitemid 27380146)
14. Bodmer JL, Meier P, Tschopp J, Schneider P. Cysteine 230 is essential for the structure and activity of the cytotoxic ligand TRAIL. J Biol Chem 2000;275:20632-7. (Pubitemid 30457649)
15. Hymowitz SG, O'Connell MP, Ultsch MH, Hurst A, Totpal K, Ashkenazi A, et al. A unique zinc-binding site revealed by a high-resolution X-ray structure of homotrimeric Apo2L/TRAIL. Biochemistry 2000;39:633-40. (Pubitemid 30065031)
16. Song JH, Tse MC, Bellail A, Phuphanich S, Khuri F, Kneteman NM, et al. 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;67:6946-55. (Pubitemid 47105542)
17. Bin L, Thorburn J, Thomas LR, Clark PE, 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;282:28189-94. (Pubitemid 47529548)
18. Kischkel FC, Lawrence DA, Chuntharapai A, Schow P, Kim KJ, Ashkenazi A. Apo2L/TRAIL-dependent recruitment of endogenous FADD and caspase-8 to death receptors 4 and 5. Immunity 2000;12:611-20.
19. Tur V, van der Sloot AM, Reis CR, Szegezdi E, Cool RH, Samali A, et al. DR4-selective tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) variants obtained by structure-based design. J Biol Chem 2008;283:20560-8.
20. van der Sloot AM, Tur V, Szegezdi E, Mullally MM, Cool RH, Samali A, et al. Designed tumor necrosis factor-related apoptosis-inducing ligand variants initiating apoptosis exclusively via the DR5 receptor. Proc Natl Acad Sci U S A 2006;103:8634-9. (Pubitemid 43878072)
21. Hellwig CT, Passante E, Rehm M. The molecular machinery regulating apoptosis signal transduction and its implication in human physiology and pathophysiologies. Curr Mol Med 2011;11:31-47.
22. Pennarun B, Meijer A, de Vries EG, Kleibeuker JH, Kruyt F, de Jong S. Playing the DISC: turning on TRAIL death receptor-mediated apoptosis in cancer. Biochim Biophys Acta 2010;1805:123-40.
23. Degli-Esposti MA, Dougall WC, Smolak PJ, Waugh JY, Smith CA, Goodwin RG. The novel receptor TRAIL-R4 induces NF-kappaB and protects against TRAIL-mediated apoptosis, yet retains an incomplete death domain. Immunity 1997;7:813-20. (Pubitemid 28064894)
24. Sheridan JP, Marsters SA, Pitti RM, Gurney A, Skubatch M, Baldwin D, et al. Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 1997;277:818-21. (Pubitemid 27366733)
25. Mérino 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;26:7046-55. (Pubitemid 44477684)
26. Emery JG, McDonnell P, Burke MB, Deen KC, Lyn S, Silverman C, et al. Osteoprotegerin is a receptor for the cytotoxic ligand TRAIL. J Biol Chem 1998;273:14363-7. (Pubitemid 28319153)
27. Kelley SK, Harris LA, Xie D, Deforge L, Totpal K, Bussiere J, et al. Preclinical studies to predict the disposition of Apo2L/tumor necrosis factor-related apoptosis-inducing ligand in humans: characterization of in vivo efficacy, pharmacokinetics, and safety. J Pharmacol Exp Ther 2001;299:31-8. (Pubitemid 32905115)
28. Tolcher AW, Mita M, Meropol NJ, von Mehren M, Patnaik A, Padavic K, et al. 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 2007;25:1390-5. (Pubitemid 46706887)
29. Bremer E, de Bruyn M, Samplonius DF, Bijma T, ten Cate B, de Leij LF, et al. Targeted delivery of a designed sTRAIL mutant results in superior apoptotic activity towards EGFR-positive tumor cells. J Mol Med (Berl) 2008;86:909-24.
30. de Bruyn M, Rybczynska AA, Wei Y, Schwenkert M, Fey GH, Dierckx RA, et al. Melanoma-associated Chondroitin Sulfate Proteoglycan (MCSP)-targeted delivery of soluble TRAIL potently inhibits melanoma outgrowth in vitro and in vivo. Mol Cancer 2010;9:301.
31. Johnstone RW, Frew AJ, Smyth MJ. The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat Rev Cancer 2008;8:782-98.
32. Jo M, Kim TH, Seol DW, Esplen JE, Dorko K, Billiar TR, et al. Apoptosis induced in normal human hepatocytes by tumor necrosis factorrelated apoptosis-inducing ligand. Nat Med 2000;6:564-7. (Pubitemid 30305907)
33. Mori E, Thomas M, Motoki K, Nakazawa K, Tahara T, Tomizuka K, et al. Human normal hepatocytes are susceptible to apoptosis signal mediated by both TRAIL-R1 and TRAIL-R2. Cell Death Differ 2004;11:203-7. (Pubitemid 38159644)
34. Nitsch R, Bechmann I, Deisz RA, Haas D, Lehmann TN, Wendling U, et al. Human brain-cell death induced by tumour-necrosis-factor-related apoptosis-inducing ligand (TRAIL). Lancet 2000;356:827-8.
35. Lawrence D, Shahrokh Z, Marsters S, Achilles K, Shih D, Mounho B, et al. Differential hepatocyte toxicity of recombinant Apo2L/TRAIL versions. Nat Med 2001;7:383-5.
36. Qin J, Chaturvedi V, Bonish B, Nickoloff BJ. Avoiding premature apoptosis of normal epidermal cells. Nat Med 2001;7:385-6. (Pubitemid 32298515)
37. Volkmann X, Fischer U, Bahr MJ, Ott M, Lehner F, Macfarlane M, et al. Increased hepatotoxicity of tumor necrosis factor-related apoptosis-inducing ligand in diseased human liver. Hepatology 2007;46:1498-508. (Pubitemid 350155532)
38. Herbst RS, Eckhardt SG, Kurzrock R, Ebbinghaus S, O'Dwyer PJ, Gordon MS, et al. Phase I dose-escalation study of recombinant human Apo2L/TRAIL, a dual proapoptotic receptor agonist, in patients with advanced cancer. J Clin Oncol 2010;28:2839-46.
39. Hotte SJ, Hirte HW, Chen EX, Siu LL, Le LH, Corey A, et al. A phase 1 study of mapatumumab (fully human monoclonal antibody to TRAILR1) in patients with advanced solid malignancies. Clin Cancer Res 2008;14:3450-5.
40. Younes A, Vose JM, Zelenetz AD, Smith MR, Burris HA, Ansell SM, et al. A Phase 1b/2 trial of mapatumumab in patients with relapsed/refractory non-Hodgkin's lymphoma. Br J Cancer 2010;103:1783-7.
41. Trarbach T, Moehler M, Heinemann V, Köhne CH, Przyborek M, Schulz C, et al. 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;102:506-12.
42. Rosevear HM, Lightfoot AJ, Griffith TS. Conatumumab, a fully human mAb against death receptor 5 for the treatment of cancer. Curr Opin Investig Drugs 2010;11:688-98.
43. Forero-Torres A, Shah J, Wood T, Posey J, Carlisle R, Copigneaux C, et al. Phase I trial of weekly tigatuzumab, an agonistic humanized monoclonal antibody targeting death receptor 5 (DR5). Cancer Biother Radiopharm 2010;25:13-9.
44. Camidge DR, Herbst RS, Gordon MS, Eckhardt SG, Kurzrock R, Durbin B, et al. A phase I safety and pharmacokinetic study of the death receptor 5 agonistic antibody PRO95780 in patients with advanced malignancies. Clin Cancer Res 2010;16:1256-63.
45. Abdulghani J, El-Deiry WS. TRAIL receptor signaling and therapeutics. Expert Opin Ther Targets 2010;14:1091-108.
46. Plummer R, Attard G, Pacey S, Li L, Razak A, Perrett R, et al. Phase 1 and pharmacokinetic study of lexatumumab in patients with advanced cancers. Clin Cancer Res 2007;13:6187-94. (Pubitemid 350075080)
47. Varfolomeev E, Maecker H, Sharp D, Lawrence D, Renz M, Vucic D, et al. Molecular determinants of kinase pathway activation by Apo2 ligand/tumor necrosis factor-related apoptosis-inducing ligand. J Biol Chem 2005;280:40599-608. (Pubitemid 41780550)
48. Ehrhardt H, Fulda S, Schmid I, Hiscott J, Debatin KM, Jeremias I. TRAIL induced survival and proliferation in cancer cells resistant towards TRAIL-induced apoptosis mediated by NF-kappaB. Oncogene 2003;22:3842-52. (Pubitemid 36819657)
49. Soria JC, Smit E, Khayat D, Besse B, Yang X, Hsu CP, et al. Phase 1b study of dulanermin (recombinant human Apo2L/TRAIL) in combination with paclitaxel, carboplatin, and bevacizumab in patients with advanced non-squamous non-small-cell lung cancer. J Clin Oncol 2010;28:1527-33.
50. Leong S, Cohen RB, Gustafson DL, Langer CJ, Camidge DR, Padavic K, et al. Mapatumumab, an antibody targeting TRAIL-R1, in combination with paclitaxel and carboplatin in patients with advanced solid malignancies: results of a phase I and pharmacokinetic study. J Clin Oncol 2009;27:4413-21.
51. Mom CH, Verweij J, Oldenhuis CN, Gietema JA, Fox NL, Miceli R, et al. Mapatumumab, a fully human agonistic monoclonal antibody that targets TRAIL-R1, in combination with gemcitabine and cisplatin: a phase I study. Clin Cancer Res 2009;15:5584-90.
52. Yu J, Zhang L. PUMA, a potent killer with or without p53. Oncogene 2008;27[Suppl 1]:S71-83.
53. Vogler M, Dinsdale D, Dyer MJ, Cohen GM. Bcl-2 inhibitors: small molecules with a big impact on cancer therapy. Cell Death Differ 2009;16:360-7.
54. Ganten TM, Haas TL, Sykora J, Stahl H, Sprick MR, Fas SC, et al. 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 2004;11[Suppl 1]:S86-96. (Pubitemid 39136801)
55. Marini P, Schmid A, Jendrossek V, Faltin H, Daniel PT, Budach W, et al. Irradiation specifically sensitises solid tumour cell lines to TRAIL mediated apoptosis. BMC Cancer 2005;5:5.
56. Guo F, Sigua C, Tao J, Bali P, George P, Li Y, et al. 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 2004;64:2580-9. (Pubitemid 38523916)
57. Shigeno M, Nakao K, Ichikawa T, Suzuki K, Kawakami A, Abiru S, et al. Interferon-alpha sensitizes human hepatoma cells to TRAIL-induced apoptosis through DR5 upregulation and NF-kappa B inactivation. Oncogene 2003;22:1653-62. (Pubitemid 36408180)
58. Herzer K, Hofmann TG, Teufel A, Schimanski CC, Moehler M, Kanzler S, et al. IFN-alpha-induced apoptosis in hepatocellular carcinoma involves promyelocytic leukemia protein and TRAIL independently of p53. Cancer Res 2009;69:855-62.
59. Stefanescu R, Bassett D, Modarresi R, Santiago F, Fakruddin M, Laurence J. Synergistic interactions between interferon-gamma and TRAIL modulate c-FLIP in endothelial cells, mediating their lineage-specific sensitivity to thrombotic thrombocytopenic purpura plasma-associated apoptosis. Blood 2008;112:340-9.
60. Brancolini C. Inhibitors of the Ubiquitin-Proteasome System and the cell death machinery: How many pathways are activated? Curr Mol Pharmacol 2008;1:24-37.
61. Cusack JC Jr, Liu R, Houston M, Abendroth K, Elliott PJ, Adams J, et al. Enhanced chemosensitivity to CPT-11 with proteasome inhibitor PS-341: implications for systemic nuclear factor-kappaB inhibition. Cancer Res 2001;61:3535-40. (Pubitemid 32694955)
62. Koschny R, Ganten TM, Sykora J, Haas TL, Sprick MR, Kolb A, et al. TRAIL/bortezomib cotreatment is potentially hepatotoxic but induces cancer-specific apoptosis within a therapeutic window. Hepatology 2007;45:649-58. (Pubitemid 46450616)
63. Voortman J, Resende TP, Abou El Hassan MA, Giaccone G, Kruyt FA. TRAIL therapy in non-small cell lung cancer cells: sensitization to death receptor-mediated apoptosis by proteasome inhibitor bortezomib. Mol Cancer Ther 2007;6:2103-12. (Pubitemid 47052501)
64. Liu X, Yue P, Chen S, Hu L, Lonial S, Khuri FR, et al. The proteasome inhibitor PS-341 (bortezomib) up-regulates DR5 expression leading to induction of apoptosis and enhancement of TRAIL-induced apoptosis despite up-regulation of c-FLIP and survivin expression in human NSCLC cells. Cancer Res 2007;67:4981-8. (Pubitemid 46910207)
65. Desagher S, Osen-Sand A, Montessuit S, Magnenat E, Vilbois F, Hochmann A, et al. Phosphorylation of bid by casein kinases I and II regulates its cleavage by caspase 8. Mol Cell. 2001;8:601-11. (Pubitemid 32946937)
66. Hellwig CT, Ludwig-Galezowska AH, Concannon CG, Litchfield DW, Prehn JH, Rehm M. Activity of protein kinase CK2 uncouples Bid cleavage from caspase-8 activation. J Cell Sci 2010;123:1401-6.
67. Cursi S, Rufini A, Stagni V, Condò I, Matafora V, Bachi A, et al. Src kinase phosphorylates Caspase-8 on Tyr380: a novel mechanism of apoptosis suppression. EMBO J 2006;25:1895-905.
68. Söderström TS, Poukkula M, Holmström TH, Heiskanen KM, Eriksson JE. Mitogen-activated protein kinase/extracellular signal-regulated kinase signaling in activated T cells abrogates TRAIL-induced apoptosis upstream of the mitochondrial amplification loop and caspase-8. J Immunol 2002;169:2851-60. (Pubitemid 35013125)
69. Harper N, Hughes MA, Farrow SN, Cohen GM, MacFarlane M. Protein kinase C modulates tumor necrosis factor-related apoptosis- inducing ligand-induced apoptosis by targeting the apical events of death receptor signaling. J Biol Chem 2003;278:44338-47. (Pubitemid 37377181)
70. Tazzari PL, Tabellini G, Ricci F, Papa V, Bortul R, Chiarini F, et al. Synergistic proapoptotic activity of recombinant TRAIL plus the Akt inhibitor Perifosine in acute myelogenous leukemia cells. Cancer Res 2008;68:9394-403.
71. Fulda S, Wick W, Weller M, Debatin KM. Smac agonists sensitize for Apo2L/TRAIL- or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat Med 2002;8:808-15.
72. Jost PJ, Grabow S, Gray D, McKenzie MD, Nachbur U, Huang DC, et al. XIAP discriminates between type I and type II FAS-induced apoptosis. Nature 2009;460:1035-9.
73. Vince JE, Wong WW, Khan N, Feltham R, Chau D, Ahmed AU, et al. IAP antagonists target cIAP1 to induce TNFalpha-dependent apoptosis. Cell 2007;131:682-93. (Pubitemid 350103599)
74. Varfolomeev E, Blankenship JW, Wayson SM, Fedorova AV, Kayagaki N, Garg P, et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis. Cell 2007;131:669-81. (Pubitemid 350087204)
75. Stadel D, Mohr A, Ref C, MacFarlane M, Zhou S, Humphreys R, et al. TRAIL-induced apoptosis is preferentially mediated via TRAIL receptor 1 in pancreatic carcinoma cells and profoundly enhanced by XIAP inhibitors. Clin Cancer Res 2010;16:5734-49.