TNF-related apoptosis-inducing ligand (trail)-armed exosomes deliver proapoptotic signals to tumor site

Clinical Cancer Research

Volumn 22, Issue 14, 2016, Pages 3499-3512

  Rivoltini, Licia ^a   Chiodoni, Claudia ^a   Squarcina, Paola ^a   Tortoreto, Monica ^a   Villa, Antonello ^b   Vergani, Barbara ^b   Bürdek, Maja ^a   Botti, Laura ^a   Arioli, Ivano ^a   Cova, Agata ^a   Mauri, Giorgio ^a   Vergani, Elisabetta ^a   Bianchi, Beatrice ^a   Mina, Pamela Della ^b   Cantone, Laura ^c   Bollati, Valentina ^c   Zaffaroni, Nadia ^a   Gianni, Alessandro Massimo ^a   Colombo, Mario Paolo ^a   Huber, Veronica ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

^b UNIVERSITY OF MILANO BICOCCA   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DEATH RECEPTOR 4; DEATH RECEPTOR 5; LENTIVIRUS VECTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; APOPTOSIS REGULATORY PROTEIN; CASPASE 3; TNFSF10 PROTEIN, HUMAN; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CONTROLLED STUDY; DRUG ACCUMULATION; DRUG CLEARANCE; EXOSOME; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LYMPHOMA; MELANOMA; MOUSE; MULTIPLE MYELOMA; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYSTEMIC THERAPY; TUMOR NECROSIS; TUMOR VOLUME; VIRAL GENE DELIVERY SYSTEM; ANIMAL; K-562 CELL LINE; METABOLISM; NECROSIS; PHYSIOLOGY; SCID MOUSE; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CASPASE 3; CELL LINE, TUMOR; EXOSOMES; FEMALE; HUMANS; K562 CELLS; MELANOMA; MICE; MICE, SCID; NECROSIS; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84978492523     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-2170     Document Type: Article

References (50)

1. Lemke J, von Karstedt S, Zinngrebe J, Walczak H. Getting TRAIL back on track for cancer therapy. Cell Death Differ 2014;21:1350-64.
2. Fuchs CS, Fakih M, Schwartzberg L, Cohn AL, Yee L, Dreisbach L, et al. TRAIL receptor agonist conatumumab with modified FOLFOX6 plus bevacizumab for first-line treatment of metastatic colorectal cancer: a randomized phase 1b/2 trial. Cancer 2013;119:4290-8.
3. von Pawel J, Harvey JH, Spigel DR, Dediu M, Reck M, Cebotaru CL, et al. Phase II trial of mapatumumab, a fully human agonist monoclonal antibody to tumor necrosis factor-related apoptosis-inducing ligand receptor 1 (TRAIL-R1), in combination with paclitaxel and carboplatin in patients with advanced non-small cell lung cancer. Clin Lung Cancer 2014;15:188-96.
4. Graves JD, Kordich JJ, Huang TH, Piasecki J, Bush TL, Sullivan T, et al. Apo2L/TRAIL and the death receptor 5 agonist antibody AMG 655 cooperate to promote receptor clustering and antitumor activity. Cancer Cell 2014;26:177-89.
5. Holland PM. Death receptor agonist therapies for cancer, which is the right TRAIL? Cytokine Growth Factor Rev 2014;25:185-93.
6. Jiang J, Liu X, Deng L, Zhang P, Wang G, Wang S, et al. GMP production and characterization of leucine zipper-tagged tumor necrosis factorrelated apoptosis-inducing ligand (LZ-TRAIL) for phase I clinical trial. Eur J Pharmacol 2014;740:722-32.
7. Tuthill MH, Montinaro A, Zinngrebe J, Prieske K, Draber P, Prieske S, et al. TRAIL-R2-specific antibodies and recombinant TRAIL can synergise to kill cancer cells. Oncogene 2015;34:2138-44.
8. Trivedi R, Mishra DP. Trailing TRAIL resistance: novel targets for TRAIL sensitization in cancer cells. Front Oncol 2015;5:69.
9. Abdulghani J, Allen JE, Dicker DT, Liu YY, Goldenberg D, Smith CD, et al. Sorafenib sensitizes solid tumors to Apo2L/TRAIL and Apo2L/TRAIL receptor agonist antibodies by the Jak2-Stat3-Mcl1 axis. PLoS ONE 2013:8:e75414.
10. Reagan MR, Seib FP, McMillin DW, Sage EK, Mitsiades CS, Janes SM, et al. Stem cell implants for cancer therapy: TRAIL-expressing mesenchymal stem cells target cancer cells in situ. J Breast Cancer 2012;15: 273-82.
11. Carlo-Stella C, Lavazza C, Di Nicola M, Cleris L, Longoni P, Milanesi M, et al. Antitumor activity of human CD34+ cells expressing membranebound tumor necrosis factor-related apoptosis-inducing ligand. Hum Gene Ther 2006;17:1225-40.
12. Loi M, Becherini P, Emionite L, Giacomini A, Cossu I, Destefanis E, et al. sTRAIL coupled to liposomes improves its pharmacokinetic profile and overcomes neuroblastoma tumour resistance in combination with bortezomib. J Control Release 2014;192:157-66.
13. Seifert O, Pollak N, Nusser A, Steiniger F, Rüger R, Pfizenmaier K, et al. Immuno-LipoTRAIL: targeted delivery of TRAIL-functionalized liposomal nanoparticles. Bioconjug Chem 2014;25:879-87.
14. De Miguel D, Basanez G, Sanchez D, Malo PG, Marzo I, Larrad L, et al. Liposomes decorated with Apo2L/TRAIL overcome chemoresistance of human hematologic tumor cells. Mol Pharm 2013;10:893-904.
15. Mitchell MJ, Wayne E, Rana K, Schaffer CB, King MR. TRAIL-coated leukocytes that kill cancer cells in the circulation. Proc Natl Acad Sci U S A 2014;111:930-5.
16. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 2013;200:373-83.
17. EL Andaloussi S, Mäger I, Breakefield XO, Wood MJ. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov 2013;12:347-57.
18. LötvallJ,HillAF,HochbergF,Buzas EI, Di Vizio D, Gardiner C, et al. Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles. J Extracell Vesicles 2014;3: 26913.
19. Colombo M, Raposo G, Thery C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol 2014;30:255-89.
20. Villarroya-Beltri C, Baixauli F, Gutierrez-Vazquez C, Sanchez-Madrid F, Mittelbrunn M. Sorting it out: regulation of exosome loading. Semin Cancer Biol 2014;28:3-13.
21. Webber J, Yeung V, Clayton A. Extracellular vesicles as modulators of the cancer microenvironment. Semin Cell Dev Biol 2015;40:27-34.
22. Whiteside TL. Immune modulation of T-cell and NK (natural killer) cell activities by TEXs (tumour-derived exosomes). Biochem Soc Trans 2013;41:245-51.
23. Zocco D, Ferruzzi P, Cappello F, Kuo WP, Fais S. Extracellular vesicles as shuttles of tumor biomarkers and antitumor drugs. Front Oncol 2014; 4:267.
24. Haney MJ, Klyachko NL, Zhao Y, Gupta R, Plotnikova EG, He Z, et al. Exosomes as drug delivery vehicles for Parkinson's disease therapy. J Control Release 2015;207:18-30.
25. Emanueli C, Shearn AI, Angelini GD, Sahoo S. Exosomes and exosomal miRNAs in cardiovascular protection and repair. Vascul Pharmacol 2015;71:24-30.
26. Morse MA, Garst J, Osada T, Khan S, Hobeika A, Clay TM, et al. A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer. J Transl Med 2005;3:9.
27. Escudier B, Dorval T, Chaput N, Andre F, Caby MP, Novault S, et al. Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of the first phase I clinical trial. J Transl Med 2005;3:10.
28. Pitt JM, Charrier M, Viaud S, Andre F, Besse B, Chaput N, et al. Dendritic cell-derived exosomes as immunotherapies in the fight against cancer. J Immunol 2014;193:1006-11.
29. Guenechea G, Gan OI, Inamitsu T, Dorrell C, Pereira DS, Kelly M, et al. Transduction of human CD34+ CD38 - bone marrow and cord bloodderived SCID-repopulating cells with third-generation lentiviral vectors. Mol Ther 2000;1:566-73.
30. Thery C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol 2006;Chapter 3:Unit 3.22.
31. Xin H, Li Y, Cui Y, Yang JJ, Zhang ZG, Chopp M. Systemic administration of exosomes released from mesenchymal stromal cells promote functional recovery and neurovascular plasticity after stroke in rats. Cereb Blood Flow Metab 2013;33:1711-5.
32. Liu Y, Li D, Liu Z, Zhou Y, Chu D, Li X, et al. Targeted exosome-mediated delivery of opioid receptor Mu siRNA for the treatment. Sci Rep 2015;5:17543.
33. Smyth T, Kullberg M, Malik N, Smith-Jones P, Graner MW, Anchordoquy TJ. Biodistribution and delivery efficiency of unmodified tumor-derived exosomes. J Control Release 2015;199:145-55.
34. Lavazza C, Carlo-Stella C, Giacomini A, Cleris L, Righi M, Sia D, et al. Human CD34? cells engineered to express membrane-bound tumor necrosis factor-related apoptosis-inducing ligand target both tumor cells and tumor vasculature. Blood 2010;115:2231-40.
35. Wilson NS, Yang A, Yang B, Couto S, Stern H, Gogineni A, et al. Proapoptotic activation of death receptor 5 on tumor endothelial cells disrupts the vasculature and reduces tumor growth. Cancer Cell 2012; 22:80-90.
36. Smith BD, Kasamon YL, Kowalski J, Gocke C, Murphy K, Miller CB, et al. K562/GM-CSF immunotherapy reduces tumor burden in chronic myeloid leukemia patients with residual disease on imatinib mesylate. Clin Cancer Res 2010;16:338-47.
37. Uno K, Inukai T, Kayagaki N, Goi K, Sato H, Nemoto A, et al. TNFrelated apoptosis-inducing ligand (TRAIL) frequently induces apoptosis in Philadelphia chromosome-positive leukemia cells. Blood 2003;101: 3658-67.
38. Burkhardt UE, Hainz U, Stevenson K, Goldstein NR, Pasek M, Naito M, et al. Autologous CLL cell vaccination early after transplant induces leukemia-specific T cells. J Clin Invest 2013;123:3756-65.
39. Pennati M, Sbarra S, De Cesare M, Lopergolo A, Locatelli SL, Campi E, et al. YM155 sensitizes triple-negative breast cancer to membrane-bound TRAIL through p38 MAPK- and CHOP-mediated DR5 upregulation. Int J Cancer 2015;136:299-309.
40. Ledford H. Cancer-fighting viruses win approval. Nature 2015:526; 622-3.
41. Ohno S, Takanashi M, Sudo K, Ueda S, Ishikawa A, Matsuyama N, et al. Systemically injected exosomes targeted to EGFR deliver antitumor micro-RNA to breast cancer cells. Mol Ther 2013;21:185-91.
42. Imai T, Takahashi Y, Nishikawa M, Kato K, Morishita M, Yamashita T, et al. Macrophage-dependent clearance of systemically administered B16BL6-derived exosomes from the blood circulation in mice. J Extracell Vesicles 2015;4:26238.
43. Norian LA, Kresowik TP, Rosevear HM, James BR, Rosean TR, Lightfoot AJ, et al. Eradication of metastatic renal cell carcinoma after adenovirusencoded TNF-related apoptosis-inducing ligand (TRAIL)/CpG immunotherapy. PLoS ONE 2012;7:e31085.
44. James BR,Brincks EL, Kucaba TA, BoonL, Griffith TS. Effective TRAIL-based immunotherapy requires both plasmacytoid and CD8a dendritic cells. Cancer Immunol Immunother 2014;63:685-97.
45. Kalra H, Adda CG, Liem M, Ang CS, Mechler A, Simpson RJ, et al. Comparative proteomics evaluation of plasma exosome isolation techniques and assessment of the stability of exosomes in normal human blood plasma. Proteomics 2013;13:3354-64.
46. van der Meel R, Fens MH, Vader P, van Solinge WW, Eniola-Adefeso O, Schiffelers RM. Extracellular vesicles as drug delivery systems: lessons from the liposome field. J Control Release 2014; 195:72-85.
47. Johnsen KB, Gudbergsson JM, Skov MN, Pilgaard L, Moos T, Duroux M. A comprehensive overview of exosomes as drug delivery vehicles - endogenous nanocarriers for targeted cancer therapy. Biochim Biophys Acta 2014;1846:75-87.
48. Nair PM, Flores H, Gogineni A, Marsters S, Lawrence DA, Kelley RF, et al. Enhancing the antitumor efficacy of a cell-surface death ligand by covalent membrane display. Proc Natl Acad Sci U S A 2015;112:5679-84.
49. Li J, Sharkey CC, King MR. Piperlongumine and immune cytokine TRAIL synergize to promote tumor death. Sci Rep 2015;5:9987.
50. Filipazzi P, Bürdek M,Villa A,Rivoltini L,Huber V.Recent advances on the role of tumor exosomes in immunosuppression and disease progression. Semin Cancer Biol 2012;22:342-9.