Dendritic cell-derived exosomes promote natural killer cell activation and proliferation: A role for NKG2D ligands and IL-15Rα

PLoS ONE

Volumn 4, Issue 3, 2009, Pages

  Viaud, Sophie ^a,b   Terme, Magali ^a,b   Flament, Caroline ^a,b   Taieb, Julien ^a,b,c   André, Fabrice ^a,b   Novault, Sophie ^a,b   Escudier, Bernard ^b   Robert, Caroline ^b   Caillat Zucman, Sophie ^d   Tursz, Thomas ^b   Zitvogel, Laurence ^a,b,c,e   Chaput, Nathalie ^a,b  

^a INSERM   (France)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^d HÔPITAL SAINT VINCENT DE PAUL   (France)

^e UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DENDRITIC CELL EXOSOME VACCINE; DENDRITIC CELL VACCINE; INTERLEUKIN 15 RECEPTOR ALPHA; NATURAL KILLER CELL RECEPTOR NKG2D; RECOMBINANT INTERLEUKIN 15; UNCLASSIFIED DRUG; CANCER VACCINE; KLRK1 PROTEIN, HUMAN; KLRK1 PROTEIN, MOUSE; LIGAND; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CELL MATURATION; CLINICAL ARTICLE; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CYTOKINE RELEASE; EX VIVO STUDY; EXOSOME; FEMALE; HUMAN; HUMAN CELL; IN VIVO STUDY; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; MELANOMA; METASTASIS; MOUSE; NATURAL KILLER CELL; NONHUMAN; PHASE 1 CLINICAL TRIAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; T LYMPHOCYTE ACTIVATION; ANIMAL; C57BL MOUSE; CELL LINE; CELL PROLIFERATION; CYTOLOGY; DENDRITIC CELL; IMMUNOLOGY; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; METHODOLOGY; TRANSPLANTATION;

ANIMALS; CANCER VACCINES; CELL LINE; CELL PROLIFERATION; DENDRITIC CELLS; EXOSOMES; HUMANS; IMMUNOTHERAPY; INTERLEUKIN-15 RECEPTOR ALPHA SUBUNIT; KILLER CELLS, NATURAL; LIGANDS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K;

EID: 63449129623     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004942     Document Type: Article

References (79)

1. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, et al. (2004) Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 10: 942-949.
2. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, et al. (2006) Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313: 1960-1964.
3. Pages F, Berger A, Camus M, Sanchez-Cabo F, Costes A, et al. (2005) Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 353: 2654-2666.
4. Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, et al. (2003) Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 348: 203-213.
5. Pardoll DM (1998) Cancer vaccines. Nat Med 4: 525-531.
6. Pardoll DM, Topalian SL (1998) The role of CD4+ T cell responses in antitumor immunity. Curr Opin Immunol 10: 588-594.
7. Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, et al. (2006) Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314: 126-129.
8. Rosenberg SA (1997) Cancer vaccines based on the identification of genes encoding cancer regression antigens. Immunol Today 18: 175-182.
9. Boon T, van Baren N (2003) Immunosurveillance against cancer and immunotherapy-synergy or antagonism? N Engl J Med 348: 252-254.
10. Dudley ME, Wunderlich JR, Robbins PF, Yang JC, Hwu P, et al. (2002) Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298: 850-854.
11. Hunder NN, Wallen H, Cao J, Hendricks DW, Reilly JZ, et al. (2008) Treatment of metastatic melanoma with autologous CD4+ T cells against NY-ESO-1. N Engl J Med 358: 2698-2703.
12. Dudley ME, Yang JC, Sherry R, Hughes MS, Royal R, et al. (2008) Adoptive Cell Therapy for Patients With Metastatic Melanoma: Evaluation of Intensive Myeloablative Chemoradiation Preparative Regimens. J Clin Oncol.
13. Dudley ME, Wunderlich JR, Yang JC, Sherry RM, Topalian SL, et al. (2005) Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol 23: 2346-2357.
14. Atanackovic D, Altorki NK, Cao Y, Ritter E, Ferrara CA, et al. (2008) Booster vaccination of cancer patients with MAGE-A3 protein reveals long-term immunological memory or tolerance depending on priming. Proc Natl Acad Sci U S A 105: 1650-1655.
15. Kruit WH, van Ojik HH, Brichard VG, Escudier B, Dorval T, et al. (2005) Phase 1/2 study of subcutaneous and intradermal immunization with a recombinant MAGE-3 protein in patients with detectable metastatic melanoma. Int J Cancer 117: 596-604.
16. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, et al. (2000) Immunobiology of dendritic cells. Annu Rev Immunol 18: 767-811.
17. Inaba K, Metlay JP, Crowley MT, Steinman RM (1990) Dendritic cells pulsed with protein antigens in vitro can prime antigen-specific, MHC-restricted T cells in situ. J Exp Med 172: 631-640.
18. Gilboa E (1999) The makings of a tumor rejection antigen. Immunity 11: 263-270.
19. Dhodapkar MV, Krasovsky J, Steinman RM, Bhardwaj N (2000) Mature dendritic cells boost functionally superior CD8(+) T-cell in humans without foreign helper epitopes. J Clin Invest 105: R9-R14.
20. Nestle FO, Alijagic S, Gilliet M, Sun Y, Grabbe S, et al. (1998) Vaccination of melanoma patients with peptide- or tumor lysate-pulsed dendritic cells. Nat Med 4: 328-332.
21. Schuler-Thurner B, Schultz ES, Berger TG, Weinlich G, Ebner S, et al. (2002) Rapid induction of tumor-specific type 1 T helper cells in metastatic melanoma patients by vaccination with mature, cryopreserved, peptide-loaded monocyte-derived dendritic cells. J Exp Med 195: 1279-1288.
22. Rosenberg SA, Yang JC, Restifo NP (2004) Cancer immunotherapy: moving beyond current vaccines. Nat Med 10: 909-915.
23. Rosenberg SA, Dudley ME, Restifo NP (2008) Cancer immunotherapy. N Engl J Med 359: 1072.
24. Banchereau J, Palucka AK, Dhodapkar M, Burkeholder S, Taquet N, et al. (2001) Immune and clinical responses in patients with metastatic melanoma to CD34(+) progenitor-derived dendritic cell vaccine. Cancer Res 61: 6451-6458.
25. Palucka AK, Dhodapkar MV, Paczesny S, Burkeholder S, Wittkowski KM, et al. (2003) Single injection of CD34+ progenitor-derived dendritic cell vaccine can lead to induction of T-cell immunity in patients with stage IV melanoma. J Immunother 26: 432-439.
26. Jager E, Maeurer M, Hohn H, Karbach J, Jager D, et al. (2000) Clonal expansion of Melan A-specific cytotoxic T lymphocytes in a melanoma patient responding to continued immunization with melanoma-associated peptides. Int J Cancer 86: 538-547.
27. Coulie PG, Karanikas V, Colau D, Lurquin C, Landry C, et al. (2001) A monoclonal cytolytic T-lymphocyte response observed in a melanoma patient vaccinated with a tumor-specific antigenic peptide encoded by gene MAGE-3. Proc Natl Acad Sci U S A 98: 10290-10295.
28. Chiong B, Wong R, Lee P, Delto J, Scotland R, et al. (2004) Characterization of long-term effector-memory T-cell responses in patients with resected high-risk melanoma receiving a melanoma Peptide vaccine. J Immunother 27: 368-379.
29. Brossart P, Wirths S, Stuhler G, Reichardt VL, Kanz L, et al. (2000) Induction of cytotoxic T-lymphocyte responses in vivo after vaccinations with peptide-pulsed dendritic cells. Blood 96: 3102-3108.
30. Diefenbach A, Jensen ER, Jamieson AM, Raulet DH (2001) Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 413: 165-171.
31. Ferlazzo G, Tsang ML, Moretta L, Melioli G, Steinman RM, et al. (2002) Human dendritic cells activate resting natural killer (NK) cells and are recognized via the NKp30 receptor by activated NK cells. J Exp Med 195: 343-351.
32. Terme M, Ullrich E, Delahaye NF, Chaput N, Zitvogel L (2008) Natural killer cell-directed therapies: moving from unexpected results to successful strategies. Nat Immunol 9: 486-494.
33. Mocikat R, Braumuller H, Gumy A, Egeter O, Ziegler H, et al. (2003) Natural killer cells activated by MHC class I(low) targets prime dendritic cells to induce protective CD8 T cell responses. Immunity 19: 561-569.
34. Fernandez NC, Lozier A, Flament C, Ricciardi-Castagnoli P, Bellet D, et al. (1999) Dendritic cells directly trigger NK cell functions: cross-talk relevant in innate anti-tumor immune responses in vivo. Nat Med 5: 405-411.
35. Lucas M, Schachterle W, Oberle K, Aichele P, Diefenbach A (2007) Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity 26: 503-517.
36. Terme M, Tomasello E, Maruyama K, Crepineau F, Chaput N, et al. (2004) IL-4 confers NK stimulatory capacity to murine dendritic cells: a signaling pathway involving KARAP/DAP12-triggering receptor expressed on myeloid cell 2 molecules. J Immunol 172: 5957-5966.
37. Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S (2008) Functions of natural killer cells. Nat Immunol 9: 503-510.
38. Zitvogel L, Regnault A, Lozier A, Wolfers J, Flament C, et al. (1998) Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med 4: 594-600.
39. Thery C, Duban L, Segura E, Veron P, Lantz O, et al. (2002) Indirect activation of naive CD4+ T cells by dendritic cell-derived exosomes. Nat Immunol 3: 1156-1162.
40. Andre F, Chaput N, Schartz NE, Flament C, Aubert N, et al. (2004) 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 172: 2126-2136.
41. Chaput N, Schartz NE, Andre F, Taieb J, Novault S, 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.
42. Escudier B, Dorval T, Chaput N, Andre F, Caby MP, et al. (2005) Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-Exosomes: results of the first phase I clinical trial. J Transl Med 3: 10.
43. Morse MA, Garst J, Osada T, Khan S, Hobeika A, et al. (2005) A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer. J Transl Med 3: 9.
44. Chaput N, Flament C, Viaud S, Taieb J, Roux S, et al. (2006) Dendritic cell derived-exosomes: biology and clinical implementations. J Leukoc Biol 80: 471-478.
45. Toomey JA, Gays F, Foster D, Brooks CG (2003) Cytokine requirements for the growth and development of mouse NK cells in vitro. J Leukoc Biol 74: 233-242.
46. Koka R, Burkett PR, Chien M, Chai S, Chan F, et al. (2003) Interleukin (IL)-15R [alpha]-deficient natural killer cells survive in normal but not IL-15R[alpha]-deficient mice. J Exp Med 197: 977-984.
47. Lodolce JP, Boone DL, Chai S, Swain RE, Dassopoulos T, et al. (1998) IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity 9: 669-676.
48. Guerra N, Tan YX, Joncker NT, Choy A, Gallardo F, et al. (2008) NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity 28: 571-580.
49. Watzl C (2003) The NKG2D receptor and its ligands-recognition beyond the "missing self"? Microbes Infect 5: 31-37.
50. Raulet DH (2003) Roles of the NKG2D immunoreceptor and its ligands. Nat Rev Immunol 3: 781-790.
51. Koka R, Burkett P, Chien M, Chai S, Boone DL, et al. (2004) Cutting edge: murine dendritic cells require IL-15R alpha to prime NK cells. J Immunol 173: 3594-3598.
52. Simhadri VR, Reiners KS, Hansen HP, Topolar D, Simhadri VL, et al. (2008) Dendritic cells release HLA-B-associated transcript-3 positive exosomes to regulate natural killer function. PLoS ONE 3: e3377.
53. Gastpar R, Gehrmann M, Bausero MA, Asea A, Gross C, et al. (2005) Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res 65: 5238-5247.
54. Elsner L, Muppala V, Gehrmann M, Lozano J, Malzahn D, et al. (2007) The heat shock protein HSP70 promotes mouse NK cell activity against tumors that express inducible NKG2D ligands. J Immunol 179: 5523-5533.
55. Osada T, Clay T, Hobeika A, Lyerly HK, Morse MA (2006) NK cell activation by dendritic cell vaccine: a mechanism of action for clinical activity. Cancer Immunol Immunother 55: 1122-1131.
56. Mailliard RB, Wankowicz-Kalinska A, Cai Q, Wesa A, Hilkens CM, et al. (2004) alpha-type-1 polarized dendritic cells: a novel immunization tool with optimized CTL-inducing activity. Cancer Res 64: 5934-5937.
57. Pilla L, Patuzzo R, Rivoltini L, Maio M, Pennacchioli E, et al. (2006) A phase II trial of vaccination with autologous, tumor-derived heat-shock protein peptide complexes Gp96, in combination with GM-CSF and interferon-alpha in metastatic melanoma patients. Cancer Immunol Immunother 55: 958-968.
58. Regunathan J, Chen Y, Wang D, Malarkannan S (2005) NKG2D receptor-mediated NK cell function is regulated by inhibitory Ly49 receptors. Blood 105: 233-240.
59. Oppenheim DE, Roberts SJ, Clarke SL, Filler R, Lewis JM, et al. (2005) Sustained localized expression of ligand for the activating NKG2D receptor impairs natural cytotoxicity in vivo and reduces tumor immunosurveillance. Nat Immunol 6: 928-937.
60. Groh V, Wu J, Yee C, Spies T (2002) Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 419: 734-738.
61. Ghiringhelli F, Menard C, Terme M, Flament C, Taieb J, et al. (2005) CD4+CD25+ regulatory T cells inhibit natural killer cell functions in a transforming growth factor-beta-dependent manner. J Exp Med 202: 1075-1085.
62. Salih HR, Rammensee HG, Steinle A (2002) Cutting edge: down-regulation of MICA on human tumors by proteolytic shedding. J Immunol 169: 4098-4102.
63. Liu C, Yu S, Zinn K, Wang J, Zhang L, et al. (2006) Murine mammary carcinoma exosomes promote tumor growth by suppression of NK cell function. J Immunol 176: 1375-1385.
64. Clayton A, Tabi Z (2005) Exosomes and the MICA-NKG2D system in cancer. Blood Cells Mol Dis 34: 206-213.
65. Clayton A, Mitchell JP, Court J, Linnane S, Mason MD, et al. (2008) Human tumor-derived exosomes down-modulate NKG2D expression. J Immunol 180: 7249-7258.
66. Prlic M, Blazar BR, Farrar MA, Jameson SC (2003) In vivo survival and homeostatic proliferation of natural killer cells. J Exp Med 197: 967-976.
67. Burkett PR, Koka R, Chien M, Chai S, Boone DL, et al. (2004) Coordinate expression and trans presentation of interleukin (IL)-15Ralpha and IL-15 supports natural killer cell and memory CD8+ T cell homeostasis. J Exp Med 200: 825-834.
68. Sutherland CL, Rabinovich B, Chalupny NJ, Brawand P, Miller R, et al. (2006) ULBPs, human ligands of the NKG2D receptor, stimulate tumor immunity with enhancement by IL-15. Blood 108: 1313-1319.
69. Epardaud M, Elpek KG, Rubinstein MP, Yonekura AR, Bellemare-Pelletier A, et al. (2008) Interleukin-15/interleukin-15R alpha complexes promote destruction of established tumors by reviving tumor-resident CD8+ T cells. Cancer Res 68: 2972-2983.
70. Dubois S, Patel HJ, Zhang M, Waldmann TA, Muller JR (2008) Preassociation of IL-15 with IL-15R alpha-IgG1-Fc enhances its activity on proliferation of NK and CD8+/CD44high T cells and its antitumor action. J Immunol 180: 2099-2106.
71. Martin-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, et al. (2004) Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol 5: 1260-1265.
72. Taieb J, Chaput N, Schartz N, Roux S, Novault S, et al. (2006) Chemoimmunotherapy of tumors: cyclophosphamide synergizes with exosome based vaccines. J Immunol 176: 2722-2729.
73. Viaud S, Ullrich E, Zitvogel L, Chaput N (2008) Exosomes for the treatment of human malignancies. Horm Metab Res 40: 82-88.
74. Segura E, Amigorena S, Thery C (2005) Mature dendritic cells secrete exosomes with strong ability to induce antigen-specific effector immune responses. Blood Cells Mol Dis 35: 89-93.
75. Segura E, Nicco C, Lombard B, Veron P, Raposo G, et al. (2005) ICAM-1 on exosomes from mature dendritic cells is critical for efficient naive T-cell priming. Blood 106: 216-223.
76. Sprent J (2005) Direct stimulation of naive T cells by antigen-presenting cell vesicles. Blood Cells Mol Dis 35: 17-20.
77. Lamparski HG, Metha-Damani A, Yao JY, Patel S, Hsu DH, et al. (2002) Production and characterization of clinical grade exosomes derived from dendritic cells. J Immunol Methods 270: 211-226.
78. Sallusto F, Lanzavecchia A (1994) Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/ macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med 179: 1109-1118.
79. Borg C, Terme M, Taieb J, Menard C, Flament C, et al. (2004) Novel mode of action of c-kit tyrosine kinase inhibitors leading to NK cell-dependent antitumor effects. J Clin Invest 114: 379-388.