Dendritic cells recruit T cell exosomes via exosomal LFA-1 leading to inhibition of CD8+ CTL responses through downregulation of peptide/MHC class I and Fas ligand-mediated cytotoxicity

Journal of Immunology

Volumn 185, Issue 9, 2010, Pages 5268-5278

  Xie, Yufeng ^a,b   Zhang, Haifeng ^a,b   Li, Wei ^a,b   Deng, Yulin ^a,b   Munegowda, Manjunatha Ankathatti ^a,b   Chibbar, Rajni ^b   Qureshi, Mabood ^b   Xiang, Jim ^a,b  

^a SASKATCHEWAN CANCER AGENCY   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; FAS LIGAND; INTERCELLULAR ADHESION MOLECULE 1; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; T LYMPHOCYTE RECEPTOR; HLA ANTIGEN CLASS 1; OVALBUMIN; PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DOWN REGULATION; EXOSOME; FEMALE; IN VITRO STUDY; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MELANOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; TRANSGENIC MOUSE; TRANSGENIC RAT; TUMOR IMMUNITY; ANIMAL; APOPTOSIS; CELL COMMUNICATION; CELL SEPARATION; CYTOTOXICITY; FLOW CYTOMETRY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE MUTANT; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY; ULTRACENTRIFUGATION; ULTRASTRUCTURE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CD8-POSITIVE T-LYMPHOCYTES; CELL COMMUNICATION; CELL SEPARATION; CYTOTOXICITY, IMMUNOLOGIC; DENDRITIC CELLS; DOWN-REGULATION; EXOSOMES; FAS LIGAND PROTEIN; FLOW CYTOMETRY; HISTOCOMPATIBILITY ANTIGENS CLASS I; LYMPHOCYTE ACTIVATION; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; OVALBUMIN; PEPTIDES; RATS; SIGNAL TRANSDUCTION; ULTRACENTRIFUGATION;

EID: 78149476304     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000386     Document Type: Article

References (52)

1. Zhang, X., J. R. Gordon, and J. Xiang. 2002. Advances in dendritic cell-based vaccine of cancer. Cancer Biother. Radiopharm. 17:601-619.
2. Taylor, D. D., H. D. Homesley, and G. J. Doellgast. 1980. Binding of specific peroxidase-labeled antibody to placental-type phosphatase on tumor-derived membrane fragments. Cancer Res. 40:4064-4069.
3. Théry, C., L. Zitvogel, and S. Amigorena. 2002. Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2:569-579.
4. Théry, C., M. Boussac, P. Véron, P. Ricciardi-Castagnoli, G. Raposo, J. Garin, and S. Amigorena. 2001. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J. Immunol. 166:7309-7318.
5. + T cells by dendritic cell-derived exosomes. Nat. Immunol. 3:1156-1162.
6. Hwang, I., X. Shen, and J. Sprent. 2003. Direct stimulation of naive T cells by membrane vesicles from antigen-presenting cells: distinct roles for CD54 and B7 molecules. Proc. Natl. Acad. Sci. USA 100:6670-6675.
7. Kovar, M., O. Boyman, X. Shen, I. Hwang, R. Kohler, and J. Sprent. 2006. Direct stimulation of T cells by membrane vesicles from antigen-presenting cells. Proc. Natl. Acad. Sci. USA 103:11671-11676.
8. + CTL responses and antitumor immunity than tumor cell-derived exosomes. Cell. Mol. Immunol. 3:205-211.
9. Vincent-Schneider, H., P. Stumptner-Cuvelette, D. Lankar, S. Pain, G. Raposo, P. Benaroch, and C. Bonnerot. 2002. Exosomes bearing HLA-DR1 molecules need dendritic cells to efficiently stimulate specific T cells. Int. Immunol. 14:713-722.
10. Hsu, D. H., P. Paz, G. Villaflor, A. Rivas, A. Mehta-Damani, E. Angevin, L. Zitvogel, and J. B. Le Pecq. 2003. Exosomes as a tumor vaccine: enhancing potency through direct loading of antigenic peptides. J. Immunother. 26:440-450.
11. Chaput, N., N. E. Schartz, F. André, J. Taïeb, S. Novault, P. Bonnaventure, N. Aubert, J. Bernard, F. Lemonnier, M. Merad, et al. 2004. Exosomes as potent cell-free peptide-based vaccine. II. Exosomes in CpG adjuvants efficiently prime naive Tc1 lymphocytes leading to tumor rejection. J. Immunol. 172:2137-2146.
12. Peters, P. J., J. Borst, V. Oorschot, M. Fukuda, O. Krähenbühl, J. Tschopp, J. W. Slot, and H. J. Geuze. 1991. Cytotoxic T lymphocyte granules are secretory lysosomes, containing both perforin and granzymes. J. Exp. Med. 173:1099-1109.
13. Martínez-Lorenzo, M. J., A. Anel, S. Gamen, I. Monlen, P. Lasierra, L. Larrad, A. Piñeiro, M. A. Alava, and J. Naval. 1999. Activated human T cells release bioactive Fas ligand and APO2 ligand in microvesicles. J. Immunol. 163:1274-1281.
14. Blanchard, N., D. Lankar, F. Faure, A. Regnault, C. Dumont, G. Raposo, and C. Hivroz. 2002. TCR activation of human T cells induces the production of exosomes bearing the TCR/CD3/ζ complex. J. Immunol. 168:3235-3241.
15. Nolte-'t Hoen, E. N., J. P. Wagenaar-Hilbers, P. J. Peters, B. M. Gadella, W. van Eden, and M. H. Wauben. 2004. Uptake of membrane molecules from T cells endows antigen-presenting cells with novel functional properties. Eur. J. Immunol. 34:3115-3125.
16. Monleón, I., M. J. Martínez-Lorenzo, L. Monteagudo, P. Lasierra, M. Taulés, M. Iturralde, A. Piñeiro, L. Larrad, M. A. Alava, J. Naval, and A. Anel. 2001. Differential secretion of Fas ligand-or APO2 ligand/TNF-related apoptosisinducing ligand-carrying microvesicles during activation-induced death of human T cells. J. Immunol. 167:6736-6744.
17. + T cell responses via acquired peptide-MHC class I complexes and CD80 costimulation, and IL-2 secretion. J. Immunol. 177:2976-2984.
18. + CTL responses. J. Immunol. 179:2731-2740.
19. Behrens, G. M., M. Li, G. M. Davey, J. Allison, R. A. Flavell, F. R. Carbone, and W. R. Heath. 2004. Helper requirements for generation of effector CTL to islet β cell antigens. J. Immunol. 172:5420-5426.
20. + CTL-and NK-mediated antitumor immunity than exosomes released from heat-shocked tumor cells expressing cytoplasmic HSP70. J. Cell. Mol. Med.
21. + T cell responses. J. Immunol. 182:193-206.
22. + T regulatory 1 cells to suppress antitumor immunity. J. Immunol. 175:2931-2937.
23. Pircher, H., K. Bürki, R. Lang, H. Hengartner, and R. M. Zinkernagel. 1989. Tolerance induction in double specific T-cell receptor transgenic mice varies with antigen. Nature 342:559-561.
24. Huang, J. F., Y. Yang, H. Sepulveda, W. Shi, I. Hwang, P. A. Peterson, M. R. Jackson, J. Sprent, and Z. Cai. 1999. TCR-mediated internalization of peptide-MHC complexes acquired by T cells. Science 286:952-954.
25. + T-cell apoptosis. Blood Cells Mol. Dis. 35:169-173.
26. + T cells induced by cross-presentation of self-antigens involves signaling through CD95 (Fas, Apo-1). J. Exp. Med. 188:415-420.
27. Ye, Z., K. A. Ahmed, J. Huang, Y. Xie, M. A. Munegowda, and J. Xiang. 2008. T cell precursor frequency differentially affects CTL responses under different immune conditions. Biochem. Biophys. Res. Commun. 367:427-434.
28. Ahmed, K. A., M. A. Munegowda, Y. Xie, and J. Xiang. 2008. Intercellular trogocytosis plays an important role in modulation of immune responses. Cell. Mol. Immunol. 5:261-269.
29. Game, D. S., N. J. Rogers, and R. I. Lechler. 2005. Acquisition of HLA-DR and costimulatory molecules by T cells from allogeneic antigen presenting cells. Am. J. Transplant. 5:1614-1625.
30. + T cells directly from the immunological synapse upon cellular dissociation. J. Immunol. 174:80-89.
31. Taams, L. S., W. van Eden, and M. H. Wauben. 1999. Antigen presentation by T cells versus professional antigen-presenting cells (APC): differential consequences for T cell activation and subsequent T cell-APC interactions. Eur. J. Immunol. 29:1543-1550.
32. + T cells involving acquired MHC class II:peptide complexes: another mechanism to limit clonal expansion? Blood 101:2704-2710.
33. Helft, J., A. Jacquet, N. T. Joncker, I. Grandjean, G. Dorothée, A. Kissenpfennig, B. Malissen, P. Matzinger, and O. Lantz. 2008. Antigen-specific T-T interactions regulate CD4 T-cell expansion. Blood 112:1249-1258.
34. + CTL responses and long-term T cell memory. J. Leukoc. Biol. 82:829-838.
35. He, T., C. Tang, Y. Liu, Z. Ye, X. Wu, Y. Wei, T. Moyana, and J. Xiang. 2007. Bidirectional membrane molecule transfer between dendritic and T cells. Biochem. Biophys. Res. Commun. 359:202-208.
36. + T cell priming involves two distinct mechanisms. J. Immunol. 181:3965-3973.
37. Kedl, R. M., B. C. Schaefer, J. W. Kappler, and P. Marrack. 2002. T cells downmodulate peptide-MHC complexes on APCs in vivo. Nat. Immunol. 3:27-32.
38. Russell, J. H., and T. J. Ley. 2002. Lymphocyte-mediated cytotoxicity. Annu. Rev. Immunol. 20:323-370.
39. Symes, J. C., C. Siatskas, D. H. Fowler, and J. A. Medin. 2009. Retrovirally transduced murine T lymphocytes expressing FasL mediate effective killing of prostate cancer cells. Cancer Gene Ther. 16:439-452.
40. Taylor, D. D., C. Gerçel-Taylor, K. S. Lyons, J. Stanson, and T. L. Whiteside. 2003. T-cell apoptosis and suppression of T-cell receptor/CD3-ζ by Fas ligandcontaining membrane vesicles shed from ovarian tumors. Clin. Cancer Res. 9:5113-5119.
41. Whiteside, T. L. 2005. Tumour-derived exosomes or microvesicles: another mechanism of tumour escape from the host immune system? Br. J. Cancer 92:209-211.
42. Taylor, D. D., S. Akyol, and C. Gercel-Taylor. 2006. Pregnancy-associated exosomes and their modulation of T cell signaling. J. Immunol. 176:1534-1542.
43. Alonso, R., M. C. Rodríguez, J. Pindado, E. Merino, I. Mérida, and M. Izquierdo. 2005. Diacylglycerol kinase a regulates the secretion of lethal exosomes bearing Fas ligand during activation-induced cell death of T lymphocytes. J. Biol. Chem. 280:28439-28450.
44. Alonso, R., C. Mazzeo, I. Mérida, and M. Izquierdo. 2007. A new role of diacylglycerol kinase a on the secretion of lethal exosomes bearing Fas ligand during activation-induced cell death of T lymphocytes. Biochimie 89:213-221.
45. + T lymphocytes in transgenic nonobese diabetic mice. J. Clin. Invest. 103:1201-1209.
46. Apostolou, I., Z. Hao, K. Rajewsky, and H. von Boehmer. 2003. Effective destruction of Fas-deficient insulin-producing b cells in type 1 diabetes. J. Exp. Med. 198:1103-1106.
47. Morelli, A. E., A. T. Larregina, W. J. Shufesky, M. L. Sullivan, D. B. Stolz, G. D. Papworth, A. F. Zahorchak, A. J. Logar, Z. Wang, S. C. Watkins, et al. 2004. Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood 104:3257-3266.
48. Théry, C., M. Ostrowski, and E. Segura. 2009. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9:581-593.
49. Hwang, I., J. F. Huang, H. Kishimoto, A. Brunmark, P. A. Peterson, M. R. Jackson, C. D. Surh, Z. Cai, and J. Sprent. 2000. T cells can use either T cell receptor or CD28 receptors to absorb and internalize cell surface molecules derived from antigen-presenting cells. J. Exp. Med. 191:1137-1148.
50. Kinashi, T. 2005. Intracellular signalling controlling integrin activation in lymphocytes. Nat. Rev. Immunol. 5:546-559.
51. van Kooyk, Y., P. van de Wiel-van Kemenade, P. Weder, T. W. Kuijpers, and C. G. Figdor. 1989. Enhancement of LFA-1-mediated cell adhesion by triggering through CD2 or CD3 on T lymphocytes. Nature 342:811-813.
52. Nolte-'t Hoen, E. N., S. I. Buschow, S. M. Anderton, W. Stoorvogel, and M. H. Wauben. 2009. Activated T cells recruit exosomes secreted by dendritic cells via LFA-1. Blood 113:1977-1981.