RIG-I activation induces the release of extracellular vesicles with antitumor activity

OncoImmunology

Volumn 5, Issue 10, 2016, Pages

  Daßler Plenker, Juliane ^a   Reiners, Katrin S ^b   van den Boorn, Jasper G ^a   Hansen, Hinrich P ^b   Putschli, Bastian ^a   Barnert, Sabine ^c   Schuberth Wagner, Christine ^a   Schubert, Rolf ^c   Tüting, Thomas ^a   Hallek, Michael ^b   Schlee, Martin ^a   Hartmann, Gunther ^a   Pogge von Strandmann, Elke ^b,d   Coch, Christoph ^a  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

BAG6; exosomes; extracellular vesicles; melanoma; NK cells; NKp30; RIG I

Indexed keywords

CD63 ANTIGEN; CD81 ANTIGEN; CD9 ANTIGEN; INTERFERON; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; RETINOIC ACID INDUCIBLE PROTEIN I;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL KILLING; CELL MEDIATED CYTOTOXICITY; CELL STIMULATION; CONTROLLED STUDY; EXOSOME; FLOW CYTOMETRY; GENE ACTIVATION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MELANOMA; MOUSE; NATURAL KILLER CELL; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; TUMOR GROWTH; WESTERN BLOTTING;

EID: 84991029161     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2016.1219827     Document Type: Article

References (57)

1. C.Thery, M.Ostrowski, E.Segura. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009; 9:581-93; PMID:19498381; http://dx.doi.org/10.1038/nri2567
2. J.G.van den Boorn, J.Daßler, C.Coch, M.Schlee, G.Hartmann. Exosomes as nucleic acid nanocarriers. Advanced Drug Delivery Reviews 2013; 65(3):331-5; PMID:22750807; http://dx.doi.org/10.1016/j.addr.2012.06.011
3. P.Kharaziha, S.Ceder, Q.Li, T.Panaretakis. Tumor cell-derived exosomes:A message in a bottle. Biochimica et Biophysica Acta (BBA) - Rev Cancer 2012; 1826:103-11; PMID:22503823; http://dx.doi.org/10.1016/j.bbcan.2012.03.006
4. R.Valenti, V.Huber, M.Iero, P.Filipazzi, G.Parmiani, L.Rivoltini. Tumor-released microvesicles as vehicles of immunosuppression. Cancer Res 2007; 67:2912-5; PMID:17409393; http://dx.doi.org/10.1158/0008-5472.CAN-07-0520
5. D.Xiao, J.Ohlendorf, Y.Chen, D.D.Taylor, S.N.Rai, S.Waigel, W.Zacharias, H.Hao, K.M.McMasters. Identifying mRNA, MicroRNA and protein profiles of melanoma exosomes. PLoS ONE 2012; 7:e46874; PMID:23056502; http://dx.doi.org/10.1371/journal.pone.0046874
6. S.Viaud, C.Thery, S.Ploix, T.Tursz, V.Lapierre, O.Lantz, L.Zitvogel, N.Chaput. Dendritic cell-derived exosomes for cancer immunotherapy:What's next? Cancer Res 2010; 70:1281-5; PMID:20145139; http://dx.doi.org/10.1158/0008-5472.CAN-09-3276
7. B.Besse, M.Charrier, V.Lapierre, E.Dansin, O.Lantz, D.Planchard, T.Le Chevalier, A.Livartoski, F.Barlesi, A.Laplanche et al. Dendritic Cell-derived Exosomes as Maintenance Immunotherapy after First Line Chemotherapy in NSCLC. Oncoimmunology 2015; 5:e1071008; PMID:27141373; http://dx.doi.org/10.1080/2162402X.2015.1071008
8. J.Binici, J.Hartmann, J.Herrmann, C.Schreiber, S.Beyer, G.Güler, V.Vogel, F.Tumulka, R.Abele, W.Mäntele et al. A soluble fragment of the tumor antigen BCL2-associated athanogene 6 (BAG-6) is essential and sufficient for inhibition of NKp30 receptor-dependent cytotoxicity of natural killer cells. J Biol Chem 2013; 288:34295-303; PMID:24133212; http://dx.doi.org/10.1074/jbc.M113.483602
9. E.Pogge von Strandmann, V.R.Simhadri, B.Tresckow von, S.Sasse, K.S.Reiners, H.P.Hansen, A.Rothe, B.Böll, V.L.Simhadri, P.Borchmann et al. Human Leukocyte Antigen-B-Associated Transcript 3 Is Released from Tumor Cells and Engages the NKp30 Receptor on Natural Killer Cells. Immunity 2007; 27:965-74; PMID:18055229; http://dx.doi.org/10.1016/j.immuni.2007.10.010
10. V.R.Simhadri, K.S.Reiners, H.P.Hansen, D.Topolar, V.L.Simhadri, K.Nohroudi, T.A.Kufer, A.Engert, E.Pogge von Strandmann. Dendritic Cells Release HLA-B-Associated Transcript-3 Positive Exosomes to Regulate Natural Killer Function. PLoS ONE 2008; 3:e3377; PMID:18852879; http://dx.doi.org/10.1371/journal.pone.0003377
11. K.S.Reiners, D.Topolar, A.Henke, V.R.Simhadri, J.Kessler, M.Sauer, M.Bessler, H.P.Hansen, S.Tawadros, M.Herling et al. Soluble ligands for NK cell receptors promote evasion of chronic lymphocytic leukemia cells from NK cell anti-tumor activity. Blood 2013; 121:3658-65; PMID:23509156; http://dx.doi.org/10.1182/blood-2013-01-476606
12. K.S.Reiners, J.Daßler, C.Coch, E.Pogge von Strandmann. Role of exosomes released by dendritic cells and/or by tumor targets:regulation of NK cell plasticity. Front Immunol 2014; 5:1074; PMID:24639679; http://dx.doi.org/10.3389/fimmu.2014.00091
13. P.D.Robbins, A.E.Morelli. Regulation of immune responses by extracellular vesicles. Nat Rev Immunol 2014; 14:195-208; PMID:24566916; http://dx.doi.org/10.1038/nri3622
14. H.Peinado, M.Alečković, S.Lavotshkin, I.Matei, B.Costa-Silva, G.Moreno-Bueno, M.Hergueta-Redondo, C.Williams, G.García-Santos, C.M.Ghajar et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 2012; 18:883-91; PMID:22635005; http://dx.doi.org/10.1038/nm.2753
15. M.Iero, R.Valenti, V.Huber, P.Filipazzi, G.Parmiani, S.Fais, L.Rivoltini. Tumour-released exosomes and their implications in cancer immunity. Cell Death Differ 2007; 15:80-8; PMID:17932500; http://dx.doi.org/10.1038/sj.cdd.4402237
16. T.Chen, J.Guo, M.Yang, X.Zhu, X.Cao. Chemokine-containing exosomes are released from heat-stressed tumor cells via lipid raft-dependent pathway and act as efficient tumor vaccine. J Immunol 2011; 186:2219-28; PMID:21242526; http://dx.doi.org/10.4049/jimmunol.1002991
17. L.H.Lv, Y.L.Wan, Y.Lin, W.Zhang, M.Yang, G.L.Li, H.M.Lin, C.Z.Shang, Y.J.Chen, J.Min. Anticancer drugs cause release of exosomes with heat shock proteins from human hepatocellular carcinoma cells that elicit effective natural killer cell antitumor responses in vitro. J Biol Chem 2012; 287:15874-85; PMID:22396543; http://dx.doi.org/10.1074/jbc.M112.340588
18. C.Corrado, A.M.Flugy, S.Taverna, S.Raimondo, G.Guggino, R.Karmali, G.De Leo, R.Alessandro. Carboxyamidotriazole-orotate inhibits the growth of imatinib-resistant chronic myeloid leukaemia cells and modulates exosomes-stimulated angiogenesis. PLoS ONE 2012; 7:e42310; PMID:22879938; http://dx.doi.org/10.1371/journal.pone.0042310
19. Y.Zhang, C.-L.Luo, B.-C.He, J.-M.Zhang, G.Cheng, X.-H.Wu. Exosomes derived from IL-12-anchored renal cancer cells increase induction of specific antitumor response in vitro:a novel vaccine for renal cell carcinoma. Int J Oncol 2010; 36:133-40; PMID:19956842; http://dx.doi.org/10.3892/ijo_00000484
20. M.Dreux, U.Garaigorta, B.Boyd, É.Décembre, J.Chung, C.Whitten-Bauer, S.Wieland, F.V.Chisari. Short-range exosomal transfer of viral RNA from infected cells to plasmacytoid dendritic cells triggers innate immunity. Cell Host & Microb 2012; 12:558-70; PMID:23084922; http://dx.doi.org/10.1016/j.chom.2012.08.010
21. V.Hornung, J.Ellegast, S.Kim, K.Brzozka, A.Jung, H.Kato, H.Poeck, S.Akira, K.K.Conzelmann, M.Schlee et al. 5′-Triphosphate RNA Is the Ligand for RIG-I. Science 2006; 314:994-7; PMID:17038590; http://dx.doi.org/10.1126/science.1132505
22. M.Schlee, A.Roth, V.Hornung, C.A.Hagmann, V.Wimmenauer, W.Barchet, C.Coch, M.Janke, A.Mihailovic, G.Wardle et al. Recognition of 5′ triphosphate by RIG-I helicase requires short blunt double-stranded RNA as contained in panhandle of negative-strand virus. Immunity 2009; 31:25-34; PMID:19576794; http://dx.doi.org/10.1016/j.immuni.2009.05.008
23. W.Barchet, V.Wimmenauer, M.Schlee, G.Hartmann. Accessing the therapeutic potential of immunostimulatory nucleic acids. Curr Opin Immunol 2008; 20:389-95; PMID:18652893; http://dx.doi.org/10.1016/j.coi.2008.07.007
24. R.Besch, H.Poeck, T.Hohenauer, D.Senft, G.Häcker, C.Berking, V.Hornung, S.Endres, T.Ruzicka, S.Rothenfusser et al. Proapoptotic signaling induced by RIG-I and MDA-5 results in type I interferon-independent apoptosis in human melanoma cells. J Clin Invest 2009; 119:2399-411; PMID:19620789; http://dx.doi.org/10.1172/JCI37155
25. M.Glas, C.Coch, D.Trageser, J.Daßler, M.Simon, P.Koch, J.Mertens, T.Quandel, R.Gorris, R.Reinartz et al. Targeting the cytosolic innate immune receptors RIG-I and MDA5 effectively counteracts cancer cell heterogeneity in glioblastoma. Stem Cells 2013; 31:1064-74; PMID:23390110; http://dx.doi.org/10.1002/stem.1350
26. T.Seya, J.Kasamatsu, M.Azuma, H.Shime, M.Matsumoto. Natural killer cell activation secondary to innate pattern sensing. J Innate Immun 2011; 3:264-73; PMID:21454965; http://dx.doi.org/10.1159/000326891
27. H.Poeck, R.Besch, C.Maihoefer, M.Renn, D.Tormo, S.S.Morskaya, S.Kirschnek, E.Gaffal, J.Landsberg, J.Hellmuth et al. 5′-triphosphate-siRNA:turning gene silencing and Rig-I activation against melanoma. Nat Med 2008; 14:1256-63; PMID:18978796; http://dx.doi.org/10.1038/nm.1887
28. M.G.E.O'Rourke, M.Johnson, C.Lanagan, J.See, J.Yang, J.R.Bell, G.J.Slater, B.M.Kerr, B.Crowe, D.M.Purdie et al. Durable complete clinical responses in a phase I/II trial using an autologous melanoma cell/dendritic cell vaccine. Cancer Immunol Immunother 2003; 52:387-95; PMID:12682787; http://dx.doi.org/10.1007/s00262-003-0375-x
29. F.Zhao, A.Sucker, S.Horn, C.Heeke, N.Bielefeld, B.Schrörs, A.Bicker, M.Lindemann, A.Roesch, G.Gaudernack et al. Melanoma lesions independently acquire T-cell resistance during metastatic latency. Cancer Research 2016; 76(15):4347-58; PMID:27261508; http://dx.doi.org/10.1158/0008-5472.CAN-16-0008
30. B.György, T.G.Szabó, M.Pásztói, Z.Pál, P.Misják, B.Aradi, V.László, É.Pállinger, E.Pap, Á.Kittel et al. Membrane vesicles, current state-of-the-art:emerging role of extracellular vesicles. Cell Mol Life Sci 2011; 68:2667-88; PMID:21560073; http://dx.doi.org/10.1007/s00018-011-0689-3
31. R.Crescitelli, C.Lässer, T.G.Szabó, Á.Kittel, M.Eldh, I.Dianzani, E.I.Buzás, J.Lötvall. Distinct RNA profiles in subpopulations of extracellular vesicles:apoptotic bodies, microvesicles and exosomes. J Extracel Vesicles 2013; 2:20677-; PMID:24223256; http://dx.doi.org/10.3402/jev.v2i0.20677
32. P.Duewell, A.Steger, H.Lohr, H.Bourhis, H.Hoelz, S.V.Kirchleitner, M.R.Stieg, S.Grassmann, S.Kobold, J.T.Siveke et al. RIG-I-like helicases induce immunogenic cell death of pancreatic cancer cells and sensitize tumors toward killing by CD8+ T cells. Cell Death Differ 2014; 21:1825-37; PMID:25012502; http://dx.doi.org/10.1038/cdd.2014.96
33. J.Landsberg, J.Kohlmeyer, M.Renn, T.Bald, M.Rogava, M.Cron, M.Fatho, V.Lennerz, T.Wölfel, M.Hölzel et al. Melanomas resist T-cell therapy through inflammation-induced reversible dedifferentiation. Nature 2012; 490:412-6; PMID:23051752; http://dx.doi.org/10.1038/nature11538
34. H.Peinado, S.Lavotshkin, D.Lyden. The secreted factors responsible for pre-metastatic niche formation:Old sayings and new thoughts. Semin Cancer Biol 2011; 21:139-46; PMID:21251983; http://dx.doi.org/10.1016/j.semcancer.2011.01.002
35. A.Clayton, J.P.Mitchell, J.Court, S.Linnane, M.D.Mason, Z.Tabi. Human tumor-derived exosomes down-modulate NKG2D expression. J Immunol 2008; 180:7249-58; PMID:18490724; http://dx.doi.org/10.4049/jimmunol.180.11.7249
36. C.Liu, S.Yu, K.Zinn, J.Wang, L.Zhang, Y.Jia, J.C.Kappes, S.Barnes, R.P.Kimberly, W.E.Grizzle et al. Murine mammary carcinoma exosomes promote tumor growth by suppression of NK cell function. J Immunol 2006; 176:1375-85; PMID:16424164; http://dx.doi.org/10.4049/jimmunol.176.3.1375
37. J.Skog, T.Würdinger, S.van Rijn, D.H.Meijer, L.Gainche, W.T.Curry, B.S.Carter, A.M.Krichevsky, X.O.Breakefield. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008; 10:1470-6; PMID:19011622; http://dx.doi.org/10.1038/ncb1800
38. J.L.Hood, R.S.San, S.A.Wickline. Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res 2011; 71:3792-801; PMID:21478294; http://dx.doi.org/10.1158/0008-5472.CAN-10-4455
39. A.Hoshino, B.Costa-Silva, T.-L.Shen, G.Rodrigues, A.Hashimoto, M.Tesic Mark, H.Molina, S.Kohsaka, A.Di Giannatale, S.Ceder et al. Tumour exosome integrins determine organotropic metastasis. Nature 2015; 527:329-35; PMID:26524530; http://dx.doi.org/10.1038/nature15756
40. R.Valenti. Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor- -mediated suppressive activity on T lymphocytes. Cancer Res 2006; 66:9290-8; PMID:16982774; http://dx.doi.org/10.1158/0008-5472.CAN-06-1819
41. A.J.Abusamra, Z.Zhong, X.Zheng, M.Li, T.E.Ichim, J.L.Chin, W.-P.Min. Tumor exosomes expressing Fas ligand mediate CD8+ T-cell apoptosis. Blood Cells Mol Dis 2005; 35:169-73; PMID:16081306; http://dx.doi.org/10.1016/j.bcmd.2005.07.001
42. F.Thuma, M.Zöller. Outsmart tumor exosomes to steal the cancer initiating cell its niche. Semin Cancer Biol 2014; 28:39-50; PMID:24631836; http://dx.doi.org/10.1016/j.semcancer.2014.02.011
43. J.Binici, J.Koch. BAG-6, a jack of all trades in health and disease. Cell Mol Life Sci 2014; 71:1829-37; PMID:24305946; http://dx.doi.org/10.1007/s00018-013-1522-y
44. C.S.Brandt, M.Baratin, E.C.Yi, J.Kennedy, Z.Gao, B.Fox, B.Haldeman, C.D.Ostrander, T.Kaifu, C.Chabannon et al. The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer cell receptor NKp30 in humans. J Exp Med 2009; 206:1495-503; PMID:19528259; http://dx.doi.org/10.1084/jem.20090681
45. A.Grover, A.A.Izzo. BAT3 regulates mycobacterium tuberculosis protein ESAT-6-mediated apoptosis of macrophages. PLoS ONE 2012; 7:e40836; PMID:22808273; http://dx.doi.org/10.1371/journal.pone.0040836
46. G.E.Etokebe, S.Zienolddiny, Z.Kupanovac, M.Enersen, S.Balen, V.Flego, L.Bulat-Kardum, A.Radojčić-Badovinac, V.Skaug, P.Bakke et al. Association of the FAM46A gene VNTRs and BAG6 rs3117582 SNP with non small cell lung cancer (NSCLC) in croatian and norwegian populations. PLoS ONE 2015; 10:e0122651; PMID:25884493; http://dx.doi.org/10.1371/journal.pone.0122651
47. Y.Wang, P.Broderick, E.Webb, X.Wu, J.Vijayakrishnan, A.Matakidou, M.Qureshi, Q.Dong, X.Gu, W.V.Chen et al. Common 5p15.33 and 6p21.33 variants influence lung cancer risk. Nat Genet 2008; 40:1407-9; PMID:18978787; http://dx.doi.org/10.1038/ng.273
48. I.Ivanov, K.C.Lo, L.Hawthorn, J.K.Cowell, Y.Ionov. Identifying candidate colon cancer tumor suppressor genes using inhibition of nonsense-mediated mRNA decay in colon cancer cells. Oncogene 2007; 26:2873-84; PMID:17086209; http://dx.doi.org/10.1038/sj.onc.1210098
49. L.Elsner, V.Muppala, M.Gehrmann, J.Lozano, D.Malzahn, H.Bickeböller, E.Brunner, M.Zientkowska, T.Herrmann, L.Walter et al. The Heat Shock Protein HSP70 Promotes Mouse NK Cell Activity against Tumors That Express Inducible NKG2D Ligands. J Immunol 2007; 179:5523-33; PMID:17911639; http://dx.doi.org/10.4049/jimmunol.179.8.5523
50. R.Gastpar, M.Gehrmann, M.A.Bausero, A.Asea, C.Gross, J.A.Schroeder, G.Multhoff. Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res 2005; 65:5238-47; PMID:15958569; http://dx.doi.org/10.1158/0008-5472.CAN-04-3804
51. K.Thress, J.Song, R.I.Morimoto, S.Kornbluth. Reversible inhibition of Hsp70 chaperone function by scythe and reaper. EMBO J 2001; 20:1033-41; PMID:11230127; http://dx.doi.org/10.1093/emboj/20.5.1033
52. G.I.Lancaster, M.A.Febbraio. Exosome-dependent trafficking of HSP70:a novel secretory pathway for cellular stress proteins. J Biol Chem 2005; 280:23349-55; PMID:15826944; http://dx.doi.org/10.1074/jbc.M502017200
53. D.Xiao, J.Ohlendorf, Y.Chen, D.D.Taylor, S.N.Rai, S.Waigel, W.Zacharias, H.Hao, K.M.McMasters. Identifying mRNA, MicroRNA and Protein Profiles of Melanoma Exosomes. PLoS ONE 2012; 7:e46874; PMID:23056502; http://dx.doi.org/10.1371/journal.pone.0046874
54. M.C.Boelens, T.J.Wu, B.Y.Nabet, B.Xu, Y.Qiu, T.Yoon, D.J.Azzam, C.Twyman-Saint Victor, B.Z.Wiemann, H.Ishwaran et al. Exosome transfer from stromal to breast cancer cells regulates therapy resistance pathways. - PubMed - NCBI. Cell 2014; 159:499-513; PMID:25417103; http://dx.doi.org/10.1016/j.cell.2014.09.051
55. T.Chen, X.Cao. Stress for maintaining memory:HSP70 as a mobile messenger for innate and adaptive immunity. Eur J Immunol 2010; 40:1541-4; PMID:20468008; http://dx.doi.org/10.1002/eji.201040616
56. R.Mears, R.A.Craven, S.Hanrahan, N.Totty, C.Upton, S.L.Young, P.Patel, P.J.Selby, R.E.Banks. Proteomic analysis of melanoma-derived exosomes by two-dimensional polyacrylamide gel electrophoresis and mass spectrometry. Proteomics 2004; 4:4019-31; PMID:15478216; http://dx.doi.org/10.1002/pmic.200400876
57. X.Gu, U.Erb, M.W.Büchler, M.Zöller. Improved vaccine efficacy of tumor exosome compared to tumor lysate loaded dendritic cells in mice. Int J Cancer 2015; 136:E74-84; PMID:25066479; http://dx.doi.org/10.1002/ijc.29100