Immune surveillance properties of human NK cell-derived exosomes

Journal of Immunology

Volumn 189, Issue 6, 2012, Pages 2833-2842

  Lugini, Luana ^a   Cecchetti, Serena ^a   Huber, Veronica ^b   Luciani, Francesca ^a   Macchia, Gianfranco ^a   Spadaro, Francesca ^a   Paris, Luisa ^a   Abalsamo, Laura ^a   Colone, Marisa ^a   Molinari, Agnese ^a   Podo, Franca ^a   Rivoltini, Licia ^b   Ramoni, Carlo ^a   Fais, Stefano ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CD56 ANTIGEN; FAS LIGAND; PERFORIN;

ARTICLE; BIOMIMETICS; CELL ACTIVATION; CELL MEMBRANE STEADY POTENTIAL; CELL VACUOLE; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXICITY; EXOSOME; HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; IMMUNOCOMPETENT CELL; IMMUNOSURVEILLANCE; NATURAL KILLER CELL; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PURIFICATION; TUMOR CELL LINE;

B-LYMPHOCYTE SUBSETS; BURKITT LYMPHOMA; CELL TRANSFORMATION, NEOPLASTIC; COCULTURE TECHNIQUES; EXOSOMES; FAS LIGAND PROTEIN; HUMANS; IMMUNOPHENOTYPING; JURKAT CELLS; K562 CELLS; KILLER CELLS, LYMPHOKINE-ACTIVATED; KILLER CELLS, NATURAL; MONITORING, IMMUNOLOGIC; PERFORIN;

EID: 84866152581     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101988     Document Type: Article

References (47)

1. Griffiths, G. M. 1996. Secretory lysosomes - a special mechanism of regulated secretion in haemopoietic cells. Trends Cell Biol. 6: 329-332. (Pubitemid 26283437)
2. Blott, E. J., and G. M. Griffiths. 2002. Secretory lysosomes. Nat. Rev. Mol. Cell Biol. 3: 122-131.
3. Lowin, B., M. C. Peitsch, and J. Tschopp. 1995. Perforin and granzymes: crucial effector molecules in cytolytic T lymphocyte and natural killer cell-mediated cytotoxicity. Curr. Top. Microbiol. Immunol. 198: 1-24.
4. Lettau, M., H. Schmidt, D. Kabelitz, and O. Janssen. 2007. Secretory lysosomes and their cargo in T and NK cells. Immunol. Lett. 108: 10-19. (Pubitemid 44970493)
5. Bossi, G., and G. M. Griffiths. 1999. Degranulation plays an essential part in regulating cell surface expression of Fas ligand in T cells and natural killer cells. Nat. Med. 5: 90-96. (Pubitemid 29051004)
6. Peters, P. J., H. J. Geuze, H. A. van der Donk, and J. Borst. 1990. A new model for lethal hit delivery by cytotoxic T lymphocytes. Immunol. Today 11: 28-32. (Pubitemid 20022603)
7. Théry, C., M. Ostrowski, and E. Segura. 2009. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9: 581-593.
8. Horstman, L. L., W. Jy, A. Minagar, C. J. Bidot, J. J. Jimenez, J. S. Alexander, and Y. S. Ahn. 2007. Cell-derived microparticles and exosomes in neuroinflammatory disorders. Int. Rev. Neurobiol. 79: 227-268.
9. Onlamoon, N., K. Pattanapanyasat, and A. A. Ansari. 2005. Human and non-human primate lentiviral infection and autoimmunity. Ann. N. Y. Acad. Sci. 1050: 397-409. (Pubitemid 41129459)
10. Théry, C., L. Zitvogel, and S. Amigorena. 2002. Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2: 569-579. (Pubitemid 37328732)
11. Schorey, J. S., and S. Bhatnagar. 2008. Exosome function: from tumor immunology to pathogen biology. Traffic 9: 871-881. (Pubitemid 351639493)
12. Raposo, G., H. W. Nijman, W. Stoorvogel, R. Liejendekker, C. V. Harding, C. J. Melief, and H. J. Geuze. 1996. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 183: 1161-1172. (Pubitemid 26113979)
13. Denzer, K., M. J. Kleijmeer, H. F. Heijnen, W. Stoorvogel, and H. J. Geuze. 2000. Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J. Cell Sci. 113: 3365-3374.
14. Valadi, H., K. Ekström, A. Bossios, M. Sjöstrand, J. J. Lee, and J. O. Lötvall. 2007. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9: 654-659. (Pubitemid 47214727)
15. + T cells. J. Virol. 83: 4354-4364.
16. Iero, M., R. Valenti, V. Huber, P. Filipazzi, G. Parmiani, S. Fais, and L. Rivoltini. 2008. Tumour-released exosomes and their implications in cancer immunity. Cell Death Differ. 15: 80-88. (Pubitemid 350286175)
17. Parolini, I., C. Federici, C. Raggi, L. Lugini, S. Palleschi, A. De Milito, C. Coscia, E. Iessi, M. Logozzi, A. Molinari, et al. 2009. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J. Biol. Chem. 284: 34211-34222.
18. Andreola, G., L. Rivoltini, C. Castelli, V. Huber, P. Perego, P. Deho, P. Squarcina, P. Accornero, F. Lozupone, L. Lugini, et al. 2002. Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J. Exp. Med. 195: 1303-1316. (Pubitemid 34564332)
19. Martínez-Lorenzo, M. J., A. Anel, S. Gamen, I. Monle n, 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.
20. Huber, V., S. Fais, M. Iero, L. Lugini, P. Canese, P. Squarcina, A. Zaccheddu, M. Colone, G. Arancia, M. Gentile, et al. 2005. Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: role in immune escape. Gastroenterology 128: 1796-1804. (Pubitemid 40824690)
21. Logozzi, M., A. De Milito, L. Lugini, M. Borghi, L. Calabrò, M. Spada, M. Perdicchio, M. L. Marino, C. Federici, E. Iessi, et al. 2009. High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLoS One 4: e5219.
22. Delcayre, A., H. Shu, and J. B. Le Pecq. 2005. Dendritic cell-derived exosomes in cancer immunotherapy: exploiting nature's antigen delivery pathway. Expert Rev. Anticancer Ther. 5: 537-547. (Pubitemid 40894984)
23. Le Pecq, J. B. 2005. Dexosomes as a therapeutic cancer vaccine: from bench to bedside. Blood Cells Mol. Dis. 35: 129-135.
24. Perussia, B., C. Ramoni, I. Anegon, M. C. Cuturi, J. Faust, and G. Trinchieri. 1987. Preferential proliferation of natural killer cells among peripheral blood mononuclear cells cocultured with B lymphoblastoid cell lines. Nat. Immun. Cell Growth Regul. 6: 171-188. (Pubitemid 18083744)
25. Kawakami, Y., S. Eliyahu, C. H. Delgado, P. F. Robbins, L. Rivoltini, S. L. Topalian, T. Miki, and S. A. Rosenberg. 1994. Cloning of the gene coding for a shared human melanoma antigen recognized by autologous T cells infiltrating into tumor. Proc. Natl. Acad. Sci. USA 91: 3515-3519. (Pubitemid 24139460)
26. Théry, C., S. Amigorena, G. Raposo, and A. Clayton. 2006. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. Unit 3.22.1-3.22.29.
27. Caby, M. P., D. Lankar, C. Vincendeau-Scherrer, G. Raposo, and C. Bonnerot. 2005. Exosomal-like vesicles are present in human blood plasma. Int. Immunol. 17: 879-887. (Pubitemid 41417955)
28. Derby, E., V. Reddy, W. Kopp, E. Nelson, M. Baseler, T. Sayers, and A. Malyguine. 2001. Three-color flow cytometric assay for the study of the mechanisms of cell-mediated cytotoxicity. Immunol. Lett. 78: 35-39. (Pubitemid 32709904)
29. Cecchetti, S., F. Spadaro, L. Lugini, F. Podo, and C. Ramoni. 2007. Functional role of phosphatidylcholine-specific phospholipase C in regulating CD16 membrane expression in natural killer cells. Eur. J. Immunol. 37: 2912-2922. (Pubitemid 47578310)
30. Zamai, L., E. Falcieri, G. Marhefka, and M. Vitale. 1996. Supravital exposure to propidium iodide identifies apoptotic cells in the absence of nucleosomal DNA fragmentation. Cytometry 23: 303-311.
31. Hirota, Y., T. Kuronita, H. Fujita, and Y. Tanaka. 2007. A role for Rab5 activity in the biogenesis of endosomal and lysosomal compartments. Biochem. Biophys. Res. Commun. 364: 40-47. (Pubitemid 47599443)
32. Peters, P. J., H. J. Geuze, H. A. Van der Donk, J. W. Slot, J. M. Griffith, N. J. Stam, H. C. Clevers, and J. Borst. 1989. Molecules relevant for T cell-target cell interaction are present in cytolytic granules of human T lymphocytes. Eur. J. Immunol. 19: 1469-1475. (Pubitemid 19221055)
33. Segura, E., C. Nicco, B. Lombard, P. Véron, G. Raposo, F. Batteux, S. Amigorena, and C. Théry. 2005. ICAM-1 on exosomes from mature dendritic cells is critical for efficient naive T-cell priming. Blood 106: 216-223. (Pubitemid 40967195)
34. Pende, D., C. Cantoni, P. Rivera, M. Vitale, R. Castriconi, S. Marcenaro, M. Nanni, R. Biassoni, C. Bottino, A. Moretta, and L. Moretta. 2001. Role of NKG2D in tumor cell lysis mediated by human NK cells: cooperation with natural cytotoxicity receptors and capability of recognizing tumors of nonepithelial origin. Eur. J. Immunol. 31: 1076-1086.
35. Sivori, S., D. Pende, C. Bottino, E. Marcenaro, A. Pessino, R. Biassoni, L. Moretta, and A. Moretta. 1999. NKp46 is the major triggering receptor involved in the natural cytotoxicity of fresh or cultured human NK cells. Correlation between surface density of NKp46 and natural cytotoxicity against autologous, allogeneic or xenogeneic target cells. Eur. J. Immunol. 29: 1656-1666. (Pubitemid 29224471)
36. Guerra, N., Y. X. Tan, N. T. Joncker, A. Choy, F. Gallardo, N. Xiong, S. Knoblaugh, D. Cado, N. M. Greenberg, and D. H. Raulet. 2008. NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity 28: 571-580.
37. Bauer, S., V. Groh, J. Wu, A. Steinle, J. H. Phillips, L. L. Lanier, and T. Spies. 1999. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285: 727-729.
38. Zuccato, E., E. J. Blott, O. Holt, S. Sigismund, M. Shaw, G. Bossi, and G. M. Griffiths. 2007. Sorting of Fas ligand to secretory lysosomes is regulated by mono-ubiquitylation and phosphorylation. J. Cell Sci. 120: 191-199. (Pubitemid 46206661)
39. Martínez-Lorenzo, M. J., M. A. Alava, A. Anel, A. Piñeiro, and J. Naval. 1996. Release of preformed Fas ligand in soluble form is the major factor for activation-induced death of Jurkat T cells. Immunology 89: 511-517. (Pubitemid 26419650)
40. Bradley, M., A. Zeytun, A. Rafi-Janajreh, P. S. Nagarkatti, and M. Nagarkatti. 1998. Role of spontaneous and interleukin-2-induced natural killer cell activity in the cytotoxicity and rejection of Fas+ and Fas- tumor cells. Blood 92: 4248-4255. (Pubitemid 28544341)
41. Houston, A., and J. O'Connell. 2004. The Fas signalling pathway and its role in the pathogenesis of cancer. Curr. Opin. Pharmacol. 4: 321-326. (Pubitemid 38987056)
42. Obata-Onai, A., S. Hashimoto, N. Onai, M. Kurachi, S. Nagai, K. Shizuno, T. Nagahata, and K. Matsushima. 2002. Comprehensive gene expression analysis of human NK cells and CD8+ T lymphocytes. Int. Immunol. 14: 1085-1098. (Pubitemid 35175216)
43. Hwang, J. Y., T. Ohira, I. Hirono, and T. Aoki. 2004. A pore-forming protein, perforin, from a non-mammalian organism, Japanese flounder, Paralichthys olivaceus. Immunogenetics 56: 360-367. (Pubitemid 39222768)
44. Smyth, M. J., K. Y. Thia, S. E. Street, D. MacGregor, D. I. Godfrey, and J. A. Trapani. 2000. Perforin-mediated cytotoxicity is critical for surveillance of spontaneous lymphoma. J. Exp. Med. 192: 755-760.
45. Mandelboim, O., N. Lieberman, M. Lev, L. Paul, T. I. Arnon, Y. Bushkin, D. M. Davis, J. L. Strominger, J. W. Yewdell, and A. Porgador. 2001. Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 409: 1055-1060. (Pubitemid 32204059)
46. Helmlinger, G., F. Yuan, M. Dellian, and R. K. Jain. 1997. Interstitial pH and pO2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat. Med. 3: 177-182. (Pubitemid 27064702)
47. Fischer, B., B. Müller, K. G. Fischer, N. Baur, and W. Kreutz. 2000. Acidic pH inhibits non-MHC-restricted killer cell functions. Clin. Immunol. 96: 252-263.