IFN-γ-producing human invariant NKT cells promote tumor-associated antigen-specific cytotoxic T cell responses

Journal of Immunology

Volumn 181, Issue 4, 2008, Pages 2446-2454

  Moreno, María ^a   Molling, Johan W ^a,b   Von Mensdorff Pouilly, Silvia ^a   Verheijen, René H M ^a,c   Hooijberg, Erik ^a   Kramer, Duco ^a   Reurs, Anneke W ^a   Van Den Eertwegh, Alfons J M ^a   Von Blomberg, B Mary E ^a   Scheper, Rik J ^a   Bontkes, Hetty J ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; CD1D ANTIGEN; CD4 ANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 12; MELAN A; TUMOR ANTIGEN; CANCER VACCINE; CD1 ANTIGEN; EPITOPE;

ACUTE GRANULOCYTIC LEUKEMIA; ANTIGEN EXPRESSION; ARTICLE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL EXPANSION; CELL FUNCTION; CELL PROLIFERATION; CELL STIMULATION; CELL TRANSFER; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; INTERFERON PRODUCTION; LEUKEMIA CELL LINE; NATURAL KILLER T CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ACUTE DISEASE; BIOSYNTHESIS; CELL DIFFERENTIATION; CELL LINE; CYTOTOXICITY; GENETIC TRANSDUCTION; GENETICS; HELA CELL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MELANOMA; METABOLISM; MYELOID LEUKEMIA; NATURAL KILLER CELL; PATHOLOGY; RETROVIRUS; SECRETION; T LYMPHOCYTE SUBPOPULATION; TRANSPLANTATION; TUMOR CELL LINE;

ACUTE DISEASE; ANTIGENS, CD1; CANCER VACCINES; CELL DIFFERENTIATION; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; CYTOTOXICITY, IMMUNOLOGIC; DENDRITIC CELLS; EPITOPES, T-LYMPHOCYTE; HELA CELLS; HUMANS; INTERFERON TYPE II; KILLER CELLS, NATURAL; LEUKEMIA, MYELOID; LYMPHOCYTE ACTIVATION; MELANOMA; RETROVIRIDAE; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, CYTOTOXIC; TRANSDUCTION, GENETIC;

EID: 53149134714     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.4.2446     Document Type: Article

References (52)

1. Godfrey, D. I., K. J. Hammond, L. D. Poulton, M. J. Smyth, and A. G. Baxter. 2000. NKT cells: facts, functions and fallacies. Immunol. Today 21: 573-583.
2. Zhou, D., J. Mattner, C. Cantu, III, N. Schrantz, N. Yin, Y. Gao, Y. Sagiv, K. Hudspeth, Y. P. Wu, T. Yamashita, et al. 2004. Lysosomal glycosphingolipid recognition by NKT cells. Science 306: 1786-1789.
3. Wu, D., G. W. Xing, M. A. Poles, A. Horowitz, Y. Kinjo, B. Sullivan, V. Bodmer-Narkevitch, O. Plettenburg, M. Kronenberg, M. Tsuji, et al. 2005. Bacterial glycolipids and analogs as antigens for CD1d-restricted NKT cells. Proc. Natl. Acad. Sci. USA 102: 1351-1356.
4. + natural killer T-cell cytotoxic activity: an important immune regulatory function. Exp. Hematol. 28: 276-282.
5. Zhang, A. L., P. Colmenero, U. Purath, C. Teixeira de Matos, W. Hueber, L. Klareskog, I. H. Tarner, E. G. Engleman, and K. Soderstrom. 2007. Natural killer cells trigger differentiation of monocytes into dendritic cells. Blood 110: 2484-2493.
6. Hegde, S., X. Chen, J. M. Keaton, F. Reddington, G. S. Besra, and J. E. Gumperz. 2007. NKT cells direct monocytes into a DC differentiation pathway. J. Leukocyte Biol. 81: 1224-1235.
7. + T cell responses to soluble antigen in vivo through direct interaction with dendritic cells. J. Immunol. 171: 5140-5147.
8. + T cells in vivo. J. Immunol. 170: 2540-2548.
9. Smyth, M. J., M. E. Wallace, S. L. Nutt, H. Yagita, D. I. Godfrey, and Y. Hayakawa. 2005. Sequential activation of NKT cells and NK cells provides effective innate immunotherapy of cancer. J. Exp. Med. 201: 1973-1985.
10. Godfrey, D. I., and M. Kronenberg. 2004. Going both ways: immune regulation via CD1d-dependent NKT cells. J. Clin. Invest. 114: 1379-1388.
11. Yu, K. O. A., and S. A. Porcelli. 2005. The diverse functions of CD1d-restricted NKT cells and their potential for immunotherapy. Immunol. Lett. 100: 42-55.
12. van der Vliet, H. J., J. W. Molling, B. M. von Blomberg, N. Nishi, W. Kolgen, A. J. van den Eertwegh, H. M. Pinedo, G. Giaccone, and R. J. Scheper. 2004. The immunoregulatory role of CD1d-restricted natural killer T cells in disease. Clin. Immunol. 112: 8-23.
13. + NKT cell numbers are decreased in a wide variety of diseases that are characterized by autoreactive tissue damage. Clin. Immunol. 100: 144-148.
14. + NKT cell numbers are decreased in cancer patients independent of tumor type or tumor load. Int. J. Cancer 116: 87-93.
15. Molling, J. W., J. A. E. Langius, J. A. Langendijk, C. R. Leemans, H. J. Bontkes, H. J. J. van der Vliet, B. M. E. von Blomberg, R. J. Scheper, and A. J. M. van den Eertwegh. 2007. Low levels of circulating invariant natural killer T cells predict poor clinical outcome in patients with head and neck squamous cell carcinoma. J. Clin. Oncol. 25: 862-868.
16. Tachibana, T., H. Onodera, T. Tsuruyama, A. Mori, S. Nagayama, H. Hiai, and M. Imamura. 2005. Increased intratumor Vα24-positive natural killer T cells: a prognostic factor for primary colorectal carcinomas. Clin. Cancer Res. 11: 7322-7327.
17. Metelitsa, L. S., H. W. Wu, H. Wang, Y. Yang, Z. Warsi, S. Asgharzadeh, S. Groshen, S. B. Wilson, and R. C. Seeger. 2004. Natural killer T cells infiltrate neuroblastomas expressing the chemokine CCL2. J. Exp. Med. 199: 1213-1221.
18. Lee, P. T., K. Benlagha, L. Teyton, and A. Bendelac. 2002. Distinct functional lineages of human Vα24 natural killer T cells. J. Exp. Med. 195: 637-641.
19. Gumperz, J. E., S. Miyake, T. Yamamura, and M. B. Brenner. 2002. Functionally distinct subsets of CD1d-restricted natural killer T cells revealed by CD1d tetramer staining. J. Exp. Med. 195: 625-636.
20. Metelitsa, L. S., K. I. Weinberg, P. D. Emanuel, and R. C. Seeger. 2003. Expression of CD1d by myelomonocytic leukemias provides a target for cytotoxic NKT cells. Leukemia 17: 1068-1077.
21. +Vα24NKT cells induces in vitro and in vivo apoptosis of human acute myeloid leukemia cells. Blood 97: 2067-2074.
22. Metelitsa, L. S., O. V. Naidenko, A. Kant, H. W. Wu, M. J. Loza, B. Perussia, M. Kronenberg, and R. C. Seeger. 2001. Human NKT cells mediate antitumor cytotoxicity directly by recognizing target cell CD1d with bound ligand or indirectly by producing IL-2 to activate NK cells. J. Immunol. 167: 3114-3122.
23. α14 NKT cells in IL-12-mediated rejection of tumors. Science 278: 1623-1626.
24. + T cells in IL-12-induced immune responses in vivo. J. Immunol. 160: 16-19.
25. Takeda, K., Y. Hayakawa, M. Atsuta, S. Hong, L. Van Kaer, K. Kobayashi, M. Ito, H. Yagita, and K. Okumura. 2000. Relative contribution of NK and NKT cells to the anti-metastatic activities of IL-12. Int. Immunol. 12: 909-914.
26. Kitamura, H., K. Iwakabe, T. Yahata, S. i. Nishimura, A. Ohta, Y. Ohmi, M. Sato, K. Takeda, K. Okumura, L. Van Kaer, et al. 1999. The natural killer T (NKT) cell ligand α-galactosylceramide demonstrates its immunopotentiating effect by inducing interleukin (IL)-12 production by dendritic cells and IL-12 receptor expression on NKT cells. J. Exp. Med. 189: 1121-1128.
27. + T cells. Nat. Immunol. 2: 1010-1017.
28. Ho, L. P., B. C. Urban, L. Jones, G. S. Ogg, and A. J. McMichael. 2004. CD4-CD8αα subset of CD1d-restricted NKT cells controls T cell expansion. J. Immunol. 172: 7350-7358.
29. + regulatory NKT cells suppress expansion of tumor antigen-specific CTLs. Int. Immunol. 17: 1143-1155.
30. Yssel, H., J. E. De Vries, M. Koken, W. Van Blitterswijk, and H. Spits. 1984. Serum-free medium for generation and propagation of functional human cytotoxic and helper T cell clones. J. Immunol. Methods 72: 219-227.
31. Kinsella, T. M., and G. P. Nolan. 1996. Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum. Gene Ther. 7: 1405-1413.
32. Heemskerk, M. H., M. Hoogeboom, R. A. de Paus, M. G. Kester, M. A. van der Hoorn, E. Goulmy, R. Willemze, and J. H. Falkenburg. 2003. Redirection of antileukemic reactivity of peripheral T lymphocytes using gene transfer of minor histocompatibility antigen HA-2-specific T-cell receptor complexes expressing a conserved alpha joining region. Blood 102: 3530-3540.
33. Bontkes, H. J., J. J. Ruizendaal, D. Kramer, S. J. Santegoets, R. J. Scheper, T. D. de Gruijl, C. J. L. M. Meijer, and E. Hooijberg. 2006. Constitutively active STAT5B induces cytokine independent growth of the AML derived MUTZ-3 cell line and accelerates its differentiation into mature dendritic cells. J. Immunother. 29: 188-200.
34. Santegoets, S. J., M. W. Schreurs, A. J. Masterson, Y. P. Liu, S. Goletz, H. Baumeister, E. W. Kueter, S. M. Lougheed, A. J. van den Eertwegh, R. J. Scheper, et al. 2006. In vitro priming of tumor-specific cytotoxic T lymphocytes using allogeneic dendritic cells derived from the human MUTZ-3 cell line. Cancer Immunol. Immunother. 55: 1480-1490.
35. Bontkes, H. J., D. Kramer, J. J. Ruizendaal, E. W. M. Kueter, V. F. I. van Tendeloo, C. J. L. M. Meijer, and E. Hooijberg. 2007. Dendritic cells transfected with interleukin-12 and tumor associated antigen mRNA induce high avidity cytotoxic T-cells. Gene Ther. 14: 366-375.
36. Schreurs, M. W., K. B. Scholten, E. W. Kueter, J. J. Ruizendaal, C. J. Meijer, and E. Hooijberg. 2003. In vitro generation and life span extension of human papillomavirus type 16-specific, healthy donor-derived CTL clones. J. Immunol. 171: 2912-2921.
37. van der Vliet, H. J., N. Nishi, Y. Koezuka, B. M. von Blomberg, A. J. van den Eertwegh, S. A. Porcelli, H. M. Pinedo, R. J. Scheper, and G. Giaccone. 2001. Potent expansion of human natural killer T cells using α-galactosylceramide (KRN7000)-loaded monocyte-derived dendritic cells, cultured in the presence of IL-7 and IL-15. J. Immunol. Methods 247: 61-72.
38. + precursors. Blood 100: 701-703.
39. + Langerhans cell precursor. J. Leukocyte Biol. 80: 1337-1344.
40. + natural killer T cells of healthy volunteers and cancer patients using α-galactosylceramide-loaded and environmentally instructed dendritic cells. Cancer Res. 63: 4101-4106.
41. Jeannin, P., Y. Delneste, M. Seveso, P. Life, and J. Y. Bonnefoy. 1996. IL-12 synergizes with IL-2 and other stimuli in inducing IL-10 production by human T cells. J. Immunol. 156: 3159-3165.
42. Chang, H. D., and A. N. D. Radbruch. 2007. The pro- and anti-inflammatory potential of interleukin-12. Ann. NY Acad. Sci. 1109: 40-46.
43. Fujii, S., K. Shimizu, M. Kronenberg, and R. M. Steinman. 2002. Prolonged IFN-γ-producing NKT response induced with α-galactosylceramide- loaded DCs. Nat. Immunol. 3: 867-874.
44. Giaccone, G., C. J. Punt, Y. Ando, R. Ruijter, N. Nishi, M. Peters, B. M. von Blomberg, R. J. Scheper, H. J. van der Vliet, A. J. van den Eertwegh, et al. 2002. A phase I study of the natural killer T-cell ligand α-galactosylceramide (KRN7000) in patients with solid tumors. Clin. Cancer Res. 8: 3702-3709.
45. Chang, D. H., K. Osman, J. Connolly, A. Kukreja, J. Krasovsky, M. Pack, A. Hutchinson, M. Geller, N. Liu, R. Annable, et al. 2005. Sustained expansion of NKT cells and antigen-specific T cells after injection of α-galactosyl-ceramide loaded mature dendritic cells in cancer patients. J. Exp. Med. 201: 1503-1517.
46. Bontkes, H. J., D. Kramer, J. J. Ruizendaal, C. J. L. M. Meijer, and E. Hooijberg. 2008. Tumor associated antigen and interleukin-12 mRNA transfected dendritic cells enhance effector function of natural killer cells and antigen specific T cells. Clin. Immunol. 127: 375-384.
47. Benham, A. M., and J. J. Neefjes. 1997. Proteasome activity limits the assembly of MHC class I molecules after IFN-γ stimulation. J. Immunol. 159: 5896-5904.
48. + T cell memory. J. Immunol. 179: 1190-1197.
49. - subsets of Vα24-invariant natural killer T cells in humans. Blood 104: 4150-4156.
50. Lin, H., M. Nieda, and A. J. Nicol. 2004. Differential proliferative response of NKT cell subpopulations to in vitro stimulation in presence of different cytokines. Eur. J. Immunol. 34: 2664-2671.
51. Hayakawa, Y., and M. J. Smyth. 2006. NKG2D and cytotoxic effector function in tumor immune surveillance. Semin. Immunol. 18: 176-185.
52. Motohashi, S., A. Ishikawa, E. Ishikawa, M. Otsuji, T. Iizasa, H. Hanaoka, N. Shimizu, S. Horiguchi, Y. Okamoto, S. I. Fujii, et al. 2006. A phase I study of in vitro expanded natural killer T cells in patients with advanced and recurrent non-small cell lung cancer. Clin. Cancer Res. 12: 6079-6086.