Invariant natural killer T cell-based immunotherapy for cancer

Immunotherapy

Volumn 1, Issue 1, 2009, Pages 73-82

  Motohashi, Shinichiro ^a   Nakayama, Toshinori ^a  

^a CHIBA UNIVERSITY   (Japan)

Author keywords

galactosylceramide; Cancer immunotherapy; Clinical trial; Dendritic cell; Natural killer T cell

Indexed keywords

1 O (ALPHA GALACTOPYRANOSYL) 2 HEXACOSANOYLAMINO 1,3,4 OCTADECANETRIOL; ALPHA GALACTOSYLCERAMIDE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 4; T LYMPHOCYTE RECEPTOR ALPHA CHAIN;

ANUS CANCER; CANCER IMMUNOLOGY; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL THERAPY; CELLULAR IMMUNITY; CLINICAL TRIAL; DENDRITIC CELL; FEVER; HUMAN; INNATE IMMUNITY; INTERFERON PRODUCTION; INVARIANT NATURAL KILLER T CELL LYMPHOMA; KIDNEY CARCINOMA; KIDNEY SARCOMA; LUNG CANCER; LUNG NON SMALL CELL CANCER; MELANOMA; MYELOMA; NATURAL KILLER T CELL; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; REVIEW; SHIVERING; SOLID TUMOR;

ADAPTIVE IMMUNITY; ANIMALS; CANCER VACCINES; CELL COMMUNICATION; CLINICAL TRIALS AS TOPIC; CYTOKINES; GALACTOSYLCERAMIDES; HUMANS; IMMUNITY, INNATE; IMMUNOTHERAPY, ADOPTIVE; LYMPHOCYTE ACTIVATION; NATURAL KILLER T-CELLS; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTE SUBSETS; TH1-TH2 BALANCE;

EID: 77953460077     PISSN: 1750743X     EISSN: None     Source Type: Journal    
DOI: 10.2217/1750743X.1.1.73     Document Type: Review

References (67)

1. Taniguchi M, Harada M, Kojo S, Nakayama T, Wakao H: The regulatory role of Vα14 NKT cells in innate and acquired immune response. Annu. Rev. Immunol. 21, 483-513 (2003).
2. Brigl M, Brenner MB: CD1: antigen presentation and T cell function. Annu. Rev. Immunol. 22, 817-890 (2004).
3. Bendelac A, Savage PB, Teyton L: The biology of NKT cells. Annu. Rev. Immunol. 25, 297-336 (2007).
4. Kronenberg M: Toward an understanding of NKT cell biology: progress and paradoxes. Annu. Rev. Immunol. 23, 877-900 (2005).
5. Kawano T, Cui J, Koezuka Y et al.: CD1d-restricted and TCR-mediated activation of Vα14 NKT cells by glycosylceramides. Science 278(5343), 1626-1629 (1997). (Pubitemid 27516282)
6. Brossay L, Chioda M, Burdin N et al.: CD1d-mediated recognition of an α-galactosylceramide by natural killer T cells is highly conserved through mammalian evolution. J. Exp. Med. 188(8), 1521-1528 (1998).
7. Spada FM, Koezuka Y, Porcelli SA: CD1d-restricted recognition of synthetic glycolipid antigens by human natural killer T cells. J. Exp. Med. 188(8), 1529-1534 (1998).
8. Yu KO, Porcelli SA: The diverse functions of CD1d-restricted NKT cells and their potential for immunotherapy. Immunol. Lett. 100(1), 42-55 (2005).
9. Van Kaer L: NKT cells: T lymphocytes with innate effector functions. Curr. Opin. Immunol. 19(3), 354-364 (2007).
10. Kawano T, Cui J, Koezuka Y et al.: Natural killer-like nonspecific tumor cell lysis mediated by specific ligand-activated Vα14 NKT cells. Proc. Natl Acad. Sci. USA 95(10), 5690-5693 (1998).
11. Kobayashi E, Motoki K, Uchida T, Fukushima H, Koezuka Y: KRN7000, a novel immunomodulator, and its antitumor activities. Oncol. Res. 7(10-11), 529-534 (1995).
12. Morita M, Motoki K, Akimoto K et al.: Structure-activity relationship of α-galactosylceramides against B16-bearing mice. J. Med. Chem. 38(12), 2176-2187 (1995).
13. Kinjo Y, Wu D, Kim G et al.: Recognition of bacterial glycosphingolipids by natural killer T cells. Nature 434(7032), 520-525 (2005). (Pubitemid 40477061)
14. Mattner J, Debord KL, Ismail N et al.: Exogenous and endogenous glycolipid antigens activate NKT cells during microbial infections. Nature 434(7032), 525-529 (2005). (Pubitemid 40477062)
15. Wilson SB, Delovitch TL: Janus-like role of regulatory iNKT cells in autoimmune disease and tumour immunity. Nat. Rev. Immunol, 3(3), 211-222 (2003).
16. Kawano T, Nakayama T, Kamada N et al.: Antitumor cytotoxicity mediated by ligand-activated human Vα24 NKT cells. Cancer Res. 59(20), 5102-5105 (1999). (Pubitemid 29503967)
17. Gumperz JE, Miyake S, Yamamura T, Brenner MB: Functionally distinct subsets of CD1d-restricted natural killer T cells revealed by CD1d tetramer staining. J. Exp. Med. 195(5), 625-636 (2002).
18. + Vα24NKT cells induces in vitro and in vivo apoptosis of human acute myeloid leukemia cells. Blood 97(7), 2067-2074 (2001).
19. + T cells and natural killer cells is essential for the antimetastatic effect of α-galactosylceramide. Blood 99(4), 1259-1266 (2002).
20. Fujii S, Shimizu K, Smith C, Bonifaz L, Steinman RM: Activation of natural killer T cells by α-galactosylceramide rapidly induces the full maturation of dendritic cells in vivo and thereby acts as an adjuvant for combined CD4 and CD8 T cell immunity to a coadministered protein. J. Exp. Med. 198(2), 267-279 (2003).
21. + T cell responses to soluble antigen in vivo through direct interaction with dendritic cells. J. Immunol. 171(10), 5140-5147 (2003).
22. + natural killer T cells mature dendritic cells, leading to strong adaptive immunity. Immunol. Rev. 220(1), 183-198 (2007).
23. Moreno M, Molling JW, von Mensdorff-Pouilly S et al.: IFN-γ-producing human invariant NKT cells promote tumor-associated antigen-specific cytotoxic T cell responses. J. Immunol. 181(4), 2446-2454 (2008).
24. Fujii S, Liu K, Smith C, Bonito AJ, Steinman RM: The linkage of innate to adaptive immunity via maturing dendritic cells in vivo requires CD40 ligation in addition to antigen presentation and CD80/86 costimulation. J. Exp. Med. 199(12), 1607-1618 (2004).
25. Taniguchi M, Seino K, Nakayama T: The NKT cell system: bridging innate and acquired immunity. Nat. Immunol. 4(12), 1164-1165 (2003).
26. Motohashi S, Kobayashi S, Ito T et al.: Preserved IFN-γ production of circulating Vα24 NKT cells in primary lung cancer patients. Int. J. Cancer 102(2), 159-165 (2002). (Pubitemid 35168029)
27. van der Vliet HJ, Molling JW, von Blomberg BM et al.: The immunoregulatory role of CD1d-restricted natural killer T cells in disease. Clin. Immunol. 112(1), 8-23 (2004).
28. + NKT cell numbers are decreased in cancer patients independent of tumor type or tumor load. Int. J. Cancer 116(1), 87-93 (2005).
29. Tahir SM, Cheng O, Shaulov A et al.: Loss of IFN-γ production by invariant NK T cells in advanced cancer. J. Immunol. 167(7), 4046-4050 (2001). (Pubitemid 32910851)
30. Konishi J, Yamazaki K, Yokouchi H, Shinagawa N, Iwabuchi K, Nishimura M: The characteristics of human NKT cells in lung cancer - CD1d independent cytotoxicity against lung cancer cells by NKT cells and decreased human NKT cell response in lung cancer patients. Hum. Immunol. 65(11), 1377-1388 (2004).
31. Dhodapkar KM, Cirignano B, Chamian F et al.: Invariant natural killer T cells are preserved in patients with glioma and exhibit antitumor lytic activity following dendritic cell-mediated expansion. Int. J. Cancer 109(6), 893-899 (2004). (Pubitemid 38500746)
32. Dhodapkar MV, Geller MD, Chang DH et al.: A reversible defect in natural killer T cell function characterizes the progression of premalignant to malignant multiple myeloma. J. Exp. Med. 197(12), 1667-1676 (2003).
33. + NKT-like cell cytotoxicity in cancer patients. Immunol. Lett. 120(1-2), 65-71 (2008).
34. Molling JW, Langius JA, Langendijk JA et al.: 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(7), 862-868 (2007).
35. Fujii S, Shimizu K, Klimek V, Geller MD, Nimer SD, Dhodapkar MV: Severe and selective deficiency of interferon-γ-producing invariant natural killer T cells in patients with myelodysplastic syndromes. Br. J. Haematol. 122(4), 617-622 (2003).
36. Tachibana T, Onodera H, Tsuruyama T et al.: Increased intratumor Vα24-positive natural killer T cells: a prognostic factor for primary colorectal carcinomas. Clin. Cancer Res. 11(20), 7322-7327 (2005).
37. Metelitsa LS, Wu HW, Wang H, et al.: Natural killer T cells infiltrate neuroblastomas expressing the chemokine CCL2. J. Exp. Med. 199(9), 1213-1221 (2004).
38. Giaccone G, Punt CJ, Ando Y et al.: A Phase I study of the natural killer T-cell ligand α-galactosylceramide (KRN7000) in patients with solid tumors. Clin. Cancer Res. 8(12), 3702-3709 (2002). ■ First clinical trial of α-galactosylceramide (GalCer; KRN7000) intravenous injection with intensive immune monitoring.
39. Kojo S, Seino K, Harada M et al.: Induction of regulatory properties in dendritic cells by Vα14 NKT cells. J. Immunol. 175(6), 3648-3655 (2005). (Pubitemid 41292024)
40. Uldrich AP, Crowe NY, Kyparissoudis K et al.: NKT cell stimulation with glycolipid antigen in vivo: costimulation-dependent expansion, Bim-dependent contraction, and hyporesponsiveness to further antigenic challenge. J. Immunol. 175(5), 3092-3101 (2005).
41. Parekh VV, Wilson MT, Olivares-Villagomez D et al.: Glycolipid antigen induces long-term natural killer T cell anergy in mice. J. Clin. Invest. 115(9), 2572-2583 (2005).
42. Veldt BJ, van der Vliet HJ, von Blomberg BM et al.: Randomized placebo controlled Phase I/II trial of α-galactosylceramide for the treatment of chronic hepatitis C. J. Hepatol. 47(3), 356-365 (2007).
43. Toura I, Kawano T, Akutsu Y, Nakayama T, Ochiai T, Taniguchi M: Cutting edge: inhibition of experimental tumor metastasis by dendritic cells pulsed with α-galactosylceramide. J. Immunol. 163(5), 2387-2391 (1999). (Pubitemid 29399156)
44. Fujii S, Shimizu K, Kronenberg M, Steinman RM: Prolonged IFN-γ-producing NKT response induced with α-galactosylceramide- loaded DCs. Nat. Immunol. 3(9), 867-874 (2002).
45. Akutsu Y, Nakayama T, Harada M et al.: Expansion of lung Vα14 NKT cells by administration of α-galactosylceramide-pulsed dendritic cells. Jpn J. Cancer Res. 93(4), 397-403 (2002).
46. Ishikawa A, Motohashi S, Ishikawa E et al.: A Phase I study of α-galactosylceramide (KRN7000)-pulsed dendritic cells in patients with advanced and recurrent non-small cell lung cancer. Clin. Cancer Res. 11(5), 1910-1917 (2005). ■■ Demonstrated α-GalCer-pulsed IL-2/GM-CSF-cultured peripheral blood mononuclear cell administration induced natural killer (NK) T-cell expansion and activation in vivo.
47. + natural killer T-cell activation by α-galactosylceramide. Int. J. Cancer 117(2), 265-273 (2005). (Pubitemid 41377447)
48. Spada FM, Borriello F, Sugita M, Watts GF, Koezuka Y, Porcelli SA: Low expression level but potent antigen presenting function of CD1d on monocyte lineage cells. Eur. J. Immunol. 30(12), 3468-3477 (2000).
49. Exley M, Garcia J, Wilson SB et al.: CD1d structure and regulation on human thymocytes, peripheral blood T cells, B cells and monocytes. Immunology 100(1), 37-47 (2000). (Pubitemid 30242880)
50. Motohashi S, Nagato K, Fujisawa T, Taniguchi M, Nakayama T, Yoshino I: Phase I/II study of αGalCer-pulsed dendritic cell in patients with advanced or recurrent non-small cell lung cancer. Presented at: The 2008 ASCO Annual Meeting. Chicago, USA, 30 May-3 June 2008.
51. Uchida T, Horiguchi S, Tanaka Y et al.: Phase I study of α-galactosylceramide-pulsed antigen presenting cells administration to the nasal submucosa in unresectable or recurrent head and neck cancer. Cancer Immunol. Immunother. 57(3), 337-345 (2008). ■■ First report of α-GalCer-pulsed antigen-presenting cell therapy correlating with objective clinical response.
52. Horiguchi S, Matsuoka T, Okamoto Y et al.: Migration of tumor antigen-pulsed dendritic cells after mucosal administration in the human upper respiratory tract. J. Clin. Immunol. 27(6), 598-604 (2007).
53. + NKT cells in human subjects results in highly coordinated secondary activation of acquired and innate immunity. Blood 103(2), 383-389 (2004). ■■ Demonstrates NKT cell activation in vivo by α-GalCer-pulsed dendritic cell (DC) administration.
54. + NKT cells expand following administration of α-galactosylceramide-pulsed dendritic cells. Vox Sang. 83(3), 250-253 (2002). (Pubitemid 36807274)
55. +T-cell activation in vivo.
56. Crowe NY, Coquet JM, Berzins SP et al.: Differential antitumor immunity mediated by NKT cell subsets in vivo. J. Exp. Med. 202(9), 1279-1288 (2005).
57. Moreno M, Molling JW, von Mensdorff-Pouilly S et al.: In vitro expanded human invariant natural killer T-cells promote functional activity of natural killer cells. Clin. Immunol. 129(1), 145-154 (2008).
58. + NKT cells by repeated stimulation with KRN7000. J. Immunol. Methods 285(2), 197-214 (2004).
59. Motohashi S, Ishikawa A, Ishikawa E et al.: 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(20 Pt 1), 6079-6086 (2006).
60. Lee PT, Benlagha K, Teyton L, Bendelac A: Distinct functional lineages of human Vα24 natural killer T cells. J. Exp. Med. 195(5), 637-641 (2002).
61. Motohashi S, Nakayama T: Clinical applications of natural killer T cell-based immunotherapy for cancer. Cancer Sci. 99(4), 638-645 (2008).
62. Chung Y, Kim BS, Kim YJ et al.: CD1d-restricted T cells license B cells to generate long-lasting cytotoxic antitumor immunity in vivo. Cancer Res. 66(13), 6843-6850 (2006). (Pubitemid 44085645)
63. Shimizu K, Kurosawa Y, Taniguchi M, Steinman RM, Fujii S: Cross-presentation of glycolipid from tumor cells loaded with α-galactosylceramide leads to potent and long-lived T cell mediated immunity via dendritic cells. J. Exp. Med. 204(11), 2641-2653 (2007).
64. Rosenberg SA, Yang JC, Restifo NP: Cancer immunotherapy: moving beyond current vaccines. Nat. Med. 10(9), 909-915 (2004).
65. Wu DY, Segal NH, Sidobre S, Kronenberg M, Chapman PB: Cross-presentation of disialoganglioside GD3 to natural killer T cells. J. Exp. Med. 198(1), 173-181 (2003).
66. NIH Consensus Statement on Management of Hepatitis C: NIH Consens. State Sci. Statements 19(3), 1-46 (2002).
67. Bochtler P, Kroger A, Schirmbeck R, Reimann J: Type I IFN-induced, NKT cell-mediated negative control of CD8 T cell priming by dendritic cells. J. Immunol. 181(3), 1633-1643 (2008).