Introduction of the CIITA gene into tumor cells produces exosomes with enhanced anti-tumor effects

Experimental and Molecular Medicine

Volumn 43, Issue 5, 2011, Pages 281-290

  Lee, Yeong Shin ^a   Kim, Soo Hyun ^a   Cho, Jung Ah ^a,b   Kim, Chul Woo ^a  

^a Seoul National University College of Medicine   (South Korea)

^b Sungkyunkwan University School of Medicine   (South Korea)

Author keywords

Cancer vaccine; CIITA; Exosomes; Im munotherapy; MHC class II molecules

Indexed keywords

CD86 ANTIGEN; CHEMOKINE RECEPTOR CCR7; GAMMA INTERFERON; IMMUNOGLOBULIN G2A ANTIBODY; INTERLEUKIN 12; INTERLEUKIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER IMMUNIZATION; CANCER INHIBITION; CANCER PREVENTION; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFICACY; EX VIVO STUDY; EXOSOME; GENETIC IMMUNIZATION; GENETIC TRANSDUCTION; IN VITRO STUDY; MELANOMA; MELANOMA CELL; MOUSE; NONHUMAN; SPLEEN CELL; TH1 CELL;

MURINAE; MUS;

EID: 79958825799     PISSN: 12263613     EISSN: 20926413     Source Type: Journal    
DOI: 10.3858/emm.2011.43.5.029     Document Type: Article

References (37)

1. André F, Chaput N, Schartz NE, Flament C, Aubert N, Bernard J, et al. Exosomes as potent cell-free peptide-based vaccine. I. Dendritic cell-derived exosomes transfer functional MHC class I/peptide complexes to dendritic cells. J Immunol 2004;172:2126-2136
2. André F, Schartz NE, Chaput N, Flament C, Raposo G, Amigorena S, Angevin E, Zitvogel L. Tumor-derived exo-somes: a new source of tumor rejection antigens. Vaccine 2002;20(Suppl 4):A28-A31
3. Andre F, Schartz NE, Movassagh M, Flament C, Pautier P, Morice P, et al. Malignant effusions and immunogenic tumour-derived exosomes. Lancet 2002;360:295-305
4. Armstrong TD, Clements VK, Martin BK, Ting JP, Ostrand-Rosenberg S. Major histocompatibility complex class II-transfected tumor cells present endogenous antigen and are potent inducers of tumor-specific immunity. Proc Natl Acad Sci USA 1997;94:6886-6891
5. Baxevanis CN, Voutsas IF, Tsitsilonis OE, Gritzapis AD, Sotiriadou R, Papamichail M. Tumor-specific CD4+ T lymphocytes from cancer patients are required for optimal induction of cytotoxic T cells against the autologous tumor. J Immunol 2000;164:3902-3912
6. Blanchard N, Lankar D, Faure F, Regnault A, Dumont C, Raposo G, Hivroz C. TCR activation of human T cells induces the production of exosomes bearing the TCR/CD3/zeta complex. J Immunol 2002;168:3235-3241
7. Cho JA, Lee YS, Kim SH, Ko JK, Kim CW. MHC independent anti-tumor immune responses induced by Hsp70-enriched exosomes generate tumor regression in murine models. Cancer Lett 2009;275:256-265
8. Cho JA, Yeo DJ, Son HY, Kim HW, Jung DS, Ko JK, Koh JS, Kim YN, Kim CW. Exosomes: a new delivery system for tumor antigens in cancer immunotherapy. Int J Cancer 2005; 114:613-622
9. Ciavarra RP. T helper cells in cytotoxic T lymphocyte development: analysis of the cellular basis for deficient T helper cell function in the L3T4-independent T helper cell pathway. Cell immunol 1991;134:427-441
10. Clayton A, Mitchell JP, Court J, Mason MD, Tabi Z. Human tumor-derived exosomes selectively impair lymphocyte responses to interleukin-2. Cancer Res 2007;67:7458-7466
11. Denzer K, Kleijmeer MJ, Heijnen HF, Stoorvogel W, Geuze HJ. Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci 2000;113 Pt 19:3365-3374
12. Escola JM, Kleijmeer MJ, Stoorvogel W, Griffith JM, Yoshie O, Geuze HJ. Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J Biol Chem 1998;273:20121-20127
13. Escudier B, Dorval T, Chaput N, André F, Caby MP, Novault S, et al. Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of thefirst phase I clinical trial. J Transl Med 2005;3:10
14. Hao S, Moyana T, Xiang J. Review: cancer immunotherapy by exosome-based vaccines. Cancer Biother Radiopharm 2007;22:692-703
15. Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 1999;94:3791-3799
16. Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 1987;262:9412-9420
17. Kass R, Agha J, Bellone S, Palmieri M, Canè S, Bignotti E, et al. In vitro induction of tumor-specific HLA class I-restricted CD8+ cytotoxic T lymphocytes from patients with locally advanced breast cancer by tumor antigen-pulsed auto-logous dendritic cells. J Surg Res 2003;112:189-197
18. Kern DE, Klarnet JP, Jensen MC, Greenberg PD. Requirement for recognition of class II molecules and processed tumor antigen for optimal generation of syngeneic tumor-specific class I-restricted CTL. J Immunol 1986;136:4303-4310
19. Kleijmeer MJ, Ossevoort MA, van Veen CJ, van Hellemond JJ, Neefjes JJ, Kast WM, et al. MHC class II compartments and the kinetics of antigen presentation in activated mouse spleen dendritic cells. J Immunol 1995;154:5715-5724
20. Meazza R, Comes A, Orengo AM, Ferrini S, Accolla RS. Tumor rejection by gene transfer of the MHC class II transactivator in murine mammary adenocarcinoma cells. Eur J Immunol 2003;33:1183-1192
21. 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
22. Mortara L, Frangione V, Castellani P. Irradiated CIITA-positive mammary adenocarcinoma cells act as a potent anti-tumor-preventive vaccine by inducing tumor-specific CD4+ T cell priming and CD8+ T cell effector functions. Int Immunol 2009;21:655-665
23. Mortara L, Castellani P, Meazza R, Tosi G, De Lerma Barbaro A, et al. CIITA-induced MHC class II expression in mammary adenocarcinoma leads to a Th1 polarization of the tumor microenvironment, tumor rejection, and specific antitumor memory. Clin Cancer Res 2006;12:3435
24. Nagarajan UM, Bushey A, Boss JM. Modulation of gene expression by the MHC class II transactivator. J Immunol 2002;169:5078-5088
25. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, Geuze HJ. B lymphocytes secrete antigen-presenting vesicles. J Exp Med 1996;183:1161-1172
26. Shortman K, Lahoud MH, Caminschi I. Improving vaccines by targeting antigens to dendritic cells. Exp Mol Med 2009;41:61-66
27. Skokos D, Goubran-Botros H, Roa M, Mecheri S. Immuno-regulatory properties of mast cell-derived exosomes. Mol Immunol 2002;38:1359-1362
28. Takenoyama M, Yoshino I, Eifuku R, So T, Imahayashi S, Sugaya M, et al. Successful induction of tumor-specific cytotoxic T lymphocytes from patients with non-small cell lung cancer using CD80-transfected autologous tumor cells. Jpn J Cancer Res 2001;92:309-315
29. Théry C, Boussac M, Véron P, Ricciardi-Castagnoli P, Raposo G, Garin J, Amigorena S. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol 2001;166:7309-7318
30. Théry C, Duban L, Segura E, Véron P, Lantz O, Amigorena S. Indirect activation of naive CD4+ T cells by dendritic cell-derived exosomes. Nat Immunol 2002;3:1156-1162
31. Thery C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol 2002;2:569-579
32. Thompson JA, Dissanayake SK, Ksander BR, Knutson KL, Disis ML, Ostrand-Rosenberg S. Tumor cells transduced with the MHC class II transactivator and CD80 activate tumor-specific CD4+ T cells whether or not they are silenced for invariant chain. Cancer Res 2006; 66:1147
33. Thompson JA, Srivastava MK, Bosch JJ, Clements VK, Ksander BR, Ostrand-Rosenberg S. The absence of invariant chain in MHC II cancer vaccines enhances the activation of tumor-reactive type 1 CD4+ T lymphocytes. Cancer Immunol Immunother 2008;57:389-398
34. van Niel G, Raposo G, Candalh C, Boussac M, Hershberg R, Cerf-Bensussan N, Heyman M. Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology 2001;121: 337-349
35. Wolfers J, Lozier A, Raposo G, Regnault A, Théry C, Masurier C, et al. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med 2001;7: 297-303
36. Wubbolts R, Leckie RS, Veenhuizen PT, Schwarzmann G, Möbius W, Hoernschemeyer J, Slot JW, Geuze HJ, Stoorvogel W. Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J Biol Chem 2003;278:10963-10972
37. Zitvogel L, Regnault A, Lozier A, Wolfers J, Flament C, Tenza D, Ricciardi-Castagnoli P, Raposo G, Amigorena S. Era dication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med 1998;4: 594-600