TRAIL on trial: Preclinical advances in cancer therapy

Trends in Molecular Medicine

Volumn 19, Issue 11, 2013, Pages 685-694

  Stuckey, Daniel W ^a   Shah, Khalid ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

Apoptosis; Cancer; Stem cells; Targeted therapy; TRAIL

Indexed keywords

2 (4 HYDROXYPHENYL) 4 MORPHOLINOPYRIDO[3',2':4,5]FURO[3,2 D]PYRIMIDINE; BEVACIZUMAB; CONATUMUMAB; FLUOROURACIL; FOLINIC ACID; LEXATUMUMAB; MAPATUMUMAB; OXALIPLATIN; RECOMBINANT TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TIGATUZUMAB; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

CANCER THERAPY; CLINICAL TRIAL; COLORECTAL CANCER; HUMAN; NONHUMAN; REVIEW; SOLID TUMOR; STEM CELL TRANSPLANTATION; VIRAL GENE DELIVERY SYSTEM;

APOPTOSIS; CANCER; STEM CELLS; TARGETED THERAPY; TRAIL;

ANIMALS; APOPTOSIS; CLINICAL TRIALS AS TOPIC; HUMANS; NEOPLASMS; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84886948521     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2013.08.007     Document Type: Review

References (80)

1. Jemal A., et al. Global cancer statistics. CA Cancer J. Clin. 2011, 61:69-90.
2. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
3. Ashkenazi A., et al. Ligand-based targeting of apoptosis in cancer: the potential of recombinant human apoptosis ligand 2/Tumor necrosis factor-related apoptosis-inducing ligand (rhApo2L/TRAIL). J. Clin. Oncol. 2008, 26:3621-3630.
4. Wiley S.R., et al. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 1995, 3:673-682.
5. Pitti R.M., et al. Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J. Biol. Chem. 1996, 271:12687-12690.
6. Allen J.E., El-Deiry W.S. Regulation of the human TRAIL gene. Cancer Biol. Ther. 2012, 13:1143-1151.
7. Ashkenazi A., et al. Safety and antitumor activity of recombinant soluble Apo2 ligand. J. Clin. Invest. 1999, 104:155-162.
8. Walczak H., et al. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat. Med. 1999, 5:157-163.
9. Johnstone R.W., et al. The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat. Rev. Cancer 2008, 8:782-798.
10. Fuchs Y., Steller H. Programmed cell death in animal development and disease. Cell 2011, 147:742-758.
11. Thorburn A. Death receptor-induced cell killing. Cell. Signal. 2004, 16:139-144.
12. Galluzzi L., et al. Mitochondria: master regulators of danger signalling. Nat. Rev. Mol. Cell Biol. 2012, 13:780-788.
13. Johnstone R.W., et al. Apoptosis: a link between cancer genetics and chemotherapy. Cell 2002, 108:153-164.
14. Spencer S.L., Sorger P.K. Measuring and modeling apoptosis in single cells. Cell 2011, 144:926-939.
15. Kantari C., Walczak H. Caspase-8 and bid: caught in the act between death receptors and mitochondria. Biochim. Biophys. Acta 2011, 1813:558-563.
16. Falschlehner C., et al. TRAIL signalling: decisions between life and death. Int. J. Biochem. Cell Biol. 2007, 39:1462-1475.
17. Kelley S.K., 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, 299:31-38.
18. Duiker E.W., et al. Development of a radioiodinated apoptosis-inducing ligand, rhTRAIL, and a radiolabelled agonist TRAIL receptor antibody for clinical imaging studies. Br. J. Pharmacol. 2012, 165:2203-2212.
19. Schneider P. Production of recombinant TRAIL and TRAIL receptor: Fc chimeric proteins. Methods Enzymol. 2000, 322:325-345.
20. Shah K., et al. Inducible release of TRAIL fusion proteins from a proapoptotic form for tumor therapy. Cancer Res. 2004, 64:3236-3242.
21. Ganten T.M., et al. Preclinical differentiation between apparently safe and potentially hepatotoxic applications of TRAIL either alone or in combination with chemotherapeutic drugs. Clin. Cancer Res. 2006, 12:2640-2646.
22. Berg D., et al. Enforced covalent trimerization increases the activity of the TNF ligand family members TRAIL and CD95L. Cell Death Differ. 2007, 14:2021-2034.
23. Wajant H., et al. Engineering death receptor ligands for cancer therapy. Cancer Lett. 2013, 332:163-174.
24. Muller N., et al. Superior serum half life of albumin tagged TNF ligands. Biochem. Biophys. Res. Commun. 2010, 396:793-799.
25. Kim T.H., et al. PEG-transferrin conjugated TRAIL (TNF-related apoptosis-inducing ligand) for therapeutic tumor targeting. J. Control. Release 2012, 162:422-428.
26. Kim T.H., et al. PEGylated TNF-related apoptosis-inducing ligand (TRAIL) analogues: pharmacokinetics and antitumor effects. Bioconjug. Chem. 2011, 22:1631-1637.
27. Kim H., et al. A sulfate polysaccharide/TNF-related apoptosis-inducing ligand (TRAIL) complex for the long-term delivery of TRAIL in poly(lactic-co-glycolic acid) (PLGA) microspheres. J. Pharm. Pharmacol. 2013, 65:11-21.
28. Hellwig C.T., Rehm M. TRAIL signaling and synergy mechanisms used in TRAIL-based combination therapies. Mol. Cancer Ther. 2012, 11:3-13.
29. Takeda K., et al. Combination antibody-based cancer immunotherapy. Cancer Sci. 2007, 98:1297-1302.
30. Amm H.M., et al. Combined modality therapy with TRAIL or agonistic death receptor antibodies. Cancer Biol. Ther. 2011, 11:431-449.
31. Ichikawa K., et al. Tumoricidal activity of a novel anti-human DR5 monoclonal antibody without hepatocyte cytotoxicity. Nat. Med. 2001, 7:954-960.
32. Zheng L., et al. Adeno-associated virus-mediated doxycycline-regulatable TRAIL expression suppresses growth of human breast carcinoma in nude mice. BMC Cancer 2012, 12:153.
33. Jiang M., et al. Synergistic antitumor effect of AAV-mediated TRAIL expression combined with cisplatin on head and neck squamous cell carcinoma. BMC Cancer 2011, 11:54.
34. Zhang H., et al. Adenovirus-mediated TRAIL expression and downregulation of Bcl-2 expression suppresses non-small cell lung cancer growth in vitro and in vivo. Int. J. Mol. Med. 2012, 30:358-364.
35. Norian L.A., et al. Eradication of metastatic renal cell carcinoma after adenovirus-encoded TNF-related apoptosis-inducing ligand (TRAIL)/CpG immunotherapy. PLoS ONE 2012, 7:e31085.
36. Kim C.Y., et al. Preclinical studies for pharmacokinetics and biodistribution of Ad-stTRAIL, an adenovirus delivering secretable trimeric TRAIL for gene therapy. Exp. Mol. Med. 2011, 43:580-586.
37. Zhang X., et al. The effect of lentivirus-mediated expression of tumor necrosis factor related apoptosis-inducing ligand and shRNA against Bcl-2 on the growth of lymphoma cells. Leuk. Lymphoma 2012, 53:710-717.
38. Hingtgen S.D., et al. A novel molecule integrating therapeutic and diagnostic activities reveals multiple aspects of stem cell-based therapy. Stem Cells 2010, 28:832-841.
39. Liu T.C., et al. Clinical trial results with oncolytic virotherapy: a century of promise, a decade of progress. Nat. Clin. Pract. Oncol. 2007, 4:101-117.
40. Varghese S., Rabkin S.D. Oncolytic herpes simplex virus vectors for cancer virotherapy. Cancer Gene Ther. 2002, 9:967-978.
41. Tamura K., et al. Multimechanistic tumor targeted oncolytic virus overcomes resistance in brain tumors. Mol. Ther. 2013, 21:68-77.
42. Corsten M.F., Shah K. Therapeutic stem-cells for cancer treatment: hopes and hurdles in tactical warfare. Lancet Oncol. 2008, 9:376-384.
43. Schichor C., et al. Mesenchymal stem cells and glioma cells form a structural as well as a functional syncytium in vitro. Exp. Neurol. 2012, 234:208-219.
44. Zielske S.P., et al. Radiation increases invasion of gene-modified mesenchymal stem cells into tumors. Int. J. Radiat. Oncol. Biol. Phys. 2009, 75:843-853.
45. Kim S.M., et al. Irradiation enhances the tumor tropism and therapeutic potential of tumor necrosis factor-related apoptosis-inducing ligand-secreting human umbilical cord blood-derived mesenchymal stem cells in glioma therapy. Stem Cells 2010, 28:2217-2228.
46. Shah K. Mesenchymal stem cells engineered for cancer therapy. Adv. Drug Deliv. Rev. 2012, 64:739-748.
47. Sasportas L.S., et al. Assessment of therapeutic efficacy and fate of engineered human mesenchymal stem cells for cancer therapy. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:4822-4827.
48. Choi S.A., et al. Therapeutic efficacy and safety of TRAIL-producing human adipose tissue-derived mesenchymal stem cells against experimental brainstem glioma. Neuro Oncol. 2011, 13:61-69.
49. Liu S., et al. Gene and doxorubicin co-delivery system for targeting therapy of glioma. Biomaterials 2012, 33:4907-4916.
50. Kim S.W., et al. Complete regression of metastatic renal cell carcinoma by multiple injections of engineered mesenchymal stem cells expressing dodecameric TRAIL and HSV-TK. Clin. Cancer Res. 2013, 19:415-427.
51. Martinez-Quintanilla J., et al. In vivo imaging of the therapeutic efficacy and fate of bimodal engineered stem cells in malignant brain tumors. Stem Cells 2013, 10.1002/stem.1355.
52. Hu Y.L., et al. Mesenchymal stem cells as a novel carrier for targeted delivery of gene in cancer therapy based on nonviral transfection. Mol. Pharm. 2012, 9:2698-2709.
53. Bagci-Onder T., et al. A dual PI3K/mTOR inhibitor, PI-103, cooperates with stem cell-delivered TRAIL in experimental glioma models. Cancer Res. 2011, 71:154-163.
54. Corsten M.F., et al. MicroRNA-21 knockdown disrupts glioma growth in vivo and displays synergistic cytotoxicity with neural precursor cell delivered S-TRAIL in human gliomas. Cancer Res. 2007, 67:8994-9000.
55. Loebinger M.R., et al. Mesenchymal stem cell delivery of TRAIL can eliminate metastatic cancer. Cancer Res. 2009, 69:4134-4142.
56. Lee H.J., et al. A therapeutic strategy for metastatic malignant fibrous histiocytoma through mesenchymal stromal cell-mediated TRAIL production. Ann. Surg. 2013, 257:952-960.
57. Maksimovic-Ivanic D., et al. Resistance to TRAIL and how to surmount it. Immunol. Res. 2012, 52:157-168.
58. Dimberg L.Y., et al. On the TRAIL to successful cancer therapy? Predicting and counteracting resistance against TRAIL-based therapeutics. Oncogene 2013, 32:1341-1350.
59. Li F., et al. In vitro and in vivo growth inhibition of drug-resistant ovarian carcinoma cells using a combination of cisplatin and a TRAIL-encoding retrovirus. Oncol. Lett. 2012, 4:1254-1258.
60. Sayers T.J., Murphy W.J. Combining proteasome inhibition with TNF-related apoptosis-inducing ligand (Apo2L/TRAIL) for cancer therapy. Cancer Immunol. Immunother. 2006, 55:76-84.
61. Bagci-Onder T., et al. Real-time imaging of the dynamics of death receptors and therapeutics that overcome TRAIL resistance in tumors. Oncogene 2013, 32:2818-2827.
62. Bangert A., et al. Histone deacetylase inhibitors sensitize glioblastoma cells to TRAIL-induced apoptosis by c-myc-mediated downregulation of cFLIP. Oncogene 2012, 31:4677-4688.
63. Nebbioso A., et al. Tumor-selective action of HDAC inhibitors involves TRAIL induction in acute myeloid leukemia cells. Nat. Med. 2005, 11:77-84.
64. Kauer T.M., et al. Encapsulated therapeutic stem cells implanted in the tumor resection cavity induce cell death in gliomas. Nat. Neurosci. 2012, 15:197-204.
65. Reagan M.R., et al. Stem cell implants for cancer therapy: TRAIL-expressing mesenchymal stem cells target cancer cells in situ. J. Breast Cancer 2012, 15:273-282.
66. Rahbarizadeh F., et al. Nanobody; an old concept and new vehicle for immunotargeting. Immunol. Invest. 2011, 40:299-338.
67. Holliger P., Hudson P.J. Engineered antibody fragments and the rise of single domains. Nat. Biotechnol. 2005, 23:1126-1136.
68. Muyldermans S. Single domain camel antibodies: current status. J. Biotechnol. 2001, 74:277-302.
69. Stieglmaier J., et al. Selective induction of apoptosis in leukemic B-lymphoid cells by a CD19-specific TRAIL fusion protein. Cancer Immunol. Immunother. 2008, 57:233-246.
70. van de Water J.A., et al. Therapeutic stem cells expressing variants of EGFR-specific nanobodies have antitumor effects. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:16642-16647.
71. Wheatley M.A., et al. Cellular signal transduction can be induced by TRAIL conjugated to microcapsules. J. Biomed. Mater. Res. A 2012, 100:2602-2611.
72. Perlstein B., et al. TRAIL conjugated to nanoparticles exhibits increased anti-tumor activities in glioma cells and glioma stem cells in vitro and in vivo. Neuro Oncol. 2013, 15:29-40.
73. Herbst R.S., 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, 28:2839-2846.
74. Hotte S.J., et al. A phase 1 study of mapatumumab (fully human monoclonal antibody to TRAIL-R1) in patients with advanced solid malignancies. Clin. Cancer Res. 2008, 14:3450-3455.
75. Forero-Torres A., et al. Phase I trial of weekly tigatuzumab, an agonistic humanized monoclonal antibody targeting death receptor 5 (DR5). Cancer Biother. Radiopharm. 2010, 25:13-19.
76. Wakelee H.A., et al. Phase I and pharmacokinetic study of lexatumumab (HGS-ETR2) given every 2 weeks in patients with advanced solid tumors. Ann. Oncol. 2010, 21:376-381.
77. Camidge D.R. Apomab: an agonist monoclonal antibody directed against Death Receptor 5/TRAIL-Receptor 2 for use in the treatment of solid tumors. Expert Opin. Biol. Ther. 2008, 8:1167-1176.
78. Younes A., et al. A Phase 1b/2 trial of mapatumumab in patients with relapsed/refractory non-Hodgkin's lymphoma. Br. J. Cancer 2010, 103:1783-1787.
79. Garraway L.A., Lander E.S. Lessons from the cancer genome. Cell 2013, 153:17-37.
80. Piras V., et al. Enhancing apoptosis in TRAIL-resistant cancer cells using fundamental response rules. Sci. Rep. 2011, 1:144.