Enrichment of human CD4+ Vα24/Vβ11 invariant NKT cells in intrahepatic malignant tumors

Journal of Immunology

Volumn 182, Issue 8, 2009, Pages 5140-5151

  Bricard, Gabriel ^a,d   Cesson, Valerie ^a   Devevre, Estelle ^a   Bouzourene, Hanifa ^b   Barbey, Catherine ^a   Rufer, Nathalie ^c   Im, Jin S ^d   Alves, Pedro M ^a   Martinet, Olivier ^a   Halkic, Nermin ^a   Cerottini, Jean Charles ^a,c   Romero, Pedro ^a   Porcelli, Steven A ^d   MacDonald, H Robson ^c   Speiser, Daniel E ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b UNIVERSITY INSTITUTE OF PATHOLOGY   (Switzerland)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8ALPHA ANTIGEN; CYTOKINE; UNCLASSIFIED DRUG; VALPHA24; VBETA11; CD1D ANTIGEN; CD1D PROTEIN, HUMAN; CD3 ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR;

ADULT; AGED; ARTICLE; BLOOD ANALYSIS; CANCER INHIBITION; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL CLONE; CLINICAL ARTICLE; COLON CARCINOMA; CYTOKINE PRODUCTION; EX VIVO STUDY; FEMALE; FLOW CYTOMETRY; HUMAN; LIVER CELL CARCINOMA; MALE; NATURAL KILLER T CELL; PRIORITY JOURNAL; TH2 CELL; UVEA MELANOMA; HEALTH; HELA CELL; IMMUNOLOGY; LIVER TUMOR; MIDDLE AGED; MOLECULAR CLONING;

ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, CD1D; ANTIGENS, CD3; CD4-POSITIVE T-LYMPHOCYTES; CLONING, MOLECULAR; FEMALE; HEALTH; HELA CELLS; HUMANS; LIVER NEOPLASMS; MALE; MIDDLE AGED; NATURAL KILLER T-CELLS; RECEPTORS, ANTIGEN, T-CELL;

EID: 65249176389     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0711086     Document Type: Article

References (76)

1. Godfrey, D. I., H. R. MacDonald, M. Kronenberg, M. J. Smyth, and L. Van Kaer. 2004. Opinion-NKT cells: what's in a name? Nat. Rev. Immunol. 4: 231-237.
2. Bricard, G., and S. A. Porcelli. 2007. Antigen presentation by CD1 molecules and the generation of lipid-specific T cell immunity. Cell. Mol. Life Sci. 64: 1824-1840. (Pubitemid 47093008)
3. Godfrey, D. I., and M. Kronenberg. 2004. Going both ways: immune regulation via CD1d-dependent NKT cells. J. Clin. Invest. 114: 1379-1388.
4. Gumperz, J. E. 2004. Antigen specificity of semi-invariant CD1d-restricted T cell receptors: The best of both worlds? Immunol. Cell Biol. 82: 285-294.
5. Porcelli, S., D. Gerdes, A. M. Fertig, and S. P. Balk. 1996. Human T cells expressing an invariant Vα24-JαQ TCRα are CD4- and heterogeneous with respect to TCRβ expression. Hum. Immunol. 48: 63-67. (Pubitemid 26238954)
6. Couedel, C., M. A. Peyrat, L. Brossay, Y. Koezuka, S. A. Porcelli, F. Davodeau, and M. Bonneville. 1998. Diverse CD1d-restricted reactivity patterns of human T cells bearing "invariant" AV24BV11 TCR. Eur. J. Immunol. 28: 4391-4397.
7. Davodeau, F., M. A. Peyrat, A. Necker, R. Dominici, F. Blanchard, C. Leget, J. Gaschet, P. Costa, Y. Jacques, A. Godard, et al. 1997. Close phenotypic and functional similarities between human and murine αβ T cells expressing invariant TCR α-chains. J. Immunol. 158: 5603-5611. (Pubitemid 127483962)
8. Karadimitris, A., S. Gadola, M. Altamirano, D. Brown, A. Woolfson, P. Klenerman, J. L. Chen, Y. Koezuka, I. A. G. Roberts, D. A. Price, et al. 2001. Human CD1d-glycolipid tetramers generated by in vitro oxidative refolding chromatography. Proc. Natl. Acad. Sci. USA 98: 3294-3298. (Pubitemid 32220839)
9. 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.
10. Lee, P. T., K. Benlagha, L. Teyton, and A. Bendelac. 2002. Distinct functional lineages of human Vα-24 natural killer T cells. J. Exp. Med. 195: 637-641. (Pubitemid 34461508)
11. Kita, H., O. V. Naidenko, M. Kronenberg, A. A. Ansari, P. Rogers, X. S. He, F. Koning, T. Mikayama, J. Van de Water, R. L. Coppel, et al. 2002. Quantitation and phenotypic analysis of natural killer T cells in primary biliary cirrhosis using a human mid tetramer. Gastroenterology 123: 1031-1043.
12. + T lymphocytes. J. Immunol. 168: 5514-5520.
13. Gadola, S. D., M. Koch, J. Marles-Wright, N. M. Lissin, D. Shepherd, G. Matulis, K. Harlos, P. M. Villiger, D. I. Stuart, B. K. Jakobsen, et al. 2006. Structure and binding kinetics of three different human CD1d-α- galactosylceramide-specific T cell receptors. J. Exp. Med. 203: 699-710.
14. Montoya, C. J., D. Pollard, J. Martinson, K. Kumari, C. Wasserfall, C. B. Mulder, M. T. Rugeles, M. A. Atkinson, A. L. Landay, and S. B. Wilson. 2007. Characterization of human invariant natural killer T subsets in health and disease using a novel invariant natural killer T cell-clonotypic monoclonal antibody, 6B11. Immunology 122: 1-14.
15. Exley, M. A., R. Hou, A. Shaulov, E. Tonti, P. Dellabona, G. Casorati, O. Akbari, H. O. Akman, E. A. Greenfield, J. E. Gumperz, et al. 2008. Selective activation, expansion, and monitoring of human iNKT cells with a monoclonal antibody specific for the TCR α-chain CDR3 loop. Eur. J. Immunol. 38: 1756-1766.
16. Norris, S., C. Collins, D. G. Doherty, F. Smith, G. McEntee, O. Traynor, N. Nolan, J. Hegarty, and C. O'Farrelly. 1998. Resident human hepatic lymphocytes are phenotypically different from circulating lymphocytes. J. Hepatol. 28: 84-90. (Pubitemid 28122504)
17. Vivier, E., and N. Anfossi. 2004. Inhibitory NK-cell receptors on T cells: witness of the past, actors of the future. Nat. Rev. Immunol. 4: 190-198. (Pubitemid 38339085)
18. Kim, C. H., E. C. Butcher, and B. Johnston. 2002. Distinct subsets of human Vα24-invariant NKT cells: cytokine responses and chemokine receptor expression. Trends Immunol. 23: 516-519.
19. + NK T cells activated by α-galactosylceramide- pulsed monocyte-derived dendritic cells. J. Immunol. 168: 3140-3144.
20. Galli, G., S. Nuti, S. Tavarini, L. Galli-Stampino, C. De Lalla, G. Casorati, P. Dellabona, and S. Abrignani. 2003. CD1d-restricted help to B cells by human invariant natural killer T lymphocytes. J. Exp. Med. 197: 1051-1057. (Pubitemid 36523203)
21. + NKT cell subsets with distinct cytokine-producing capacity. Blood 100: 11-16.
22. Thomas, S. Y., R. H. Hou, J. E. Boyson, T. K. Means, C. Hess, D. P. Olson, J. L. Strominger, M. B. Brenner, J. E. Gumperz, S. B. Wilson, and A. D. Luster. 2003. CD1d-restricted NKT cells express a chemokine receptor profile indicative of Th1-type inflammatory homing cells. J. Immunol. 171: 2571-2580.
23. + regulatory NKT cells suppress expansion of tumor antigen-specific CTLs. Int. Immunol. 17: 1143-1155.
24. Terabe, M., S. Matsui, N. Noben-Trauth, H. J. Chen, C. Watson, D. D. Donaldson, D. P. Carbone, W. E. Paul, and J. A. Berzofsky. 2000. NKT cell-mediated repression of tumor immunosurveillance by IL-13 and the IL-4RSTAT6 pathway. Nat. Immunol. 1: 515-520.
25. Moodycliffe, A. M., D. Nghiem, G. Clydesdale, and S. E. Ullrich. 2000. Immune suppression and skin cancer development: regulation by NKT cells. Nat. Immunol. 1: 521-525.
26. + NKT regulatory cells and IL-13. Int. J. Cancer 114: 80-87.
27. Terabe, M., J. Swann, E. Ambrosino, P. Sinha, S. Takaku, Y. Hayakawa, D. I. Godfrey, S. Ostrand-Rosenberg, M. J. Smyth, and J. A. Berzofsky. 2005. A nonclassical non-Vα14Jα18 CD1d-restricted (type II) NKT cell is sufficient for down-regulation of tumor immunosurveillance. J. Exp. Med. 202: 1627-1633. (Pubitemid 41815868)
28. Renukaradhya, G. J., V. Sriram, W. Du, J. Gervay-Hague, L. Van Kaer, and R. R. Brutkiewicz. 2006. Inhibition of antitumor immunity by invariant natural killer T cells in a T-cell lymphoma model in vivo. Int. J. Cancer. 118: 3045-3053.
29. Crowe, N. Y., J. M. Coquet, S. P. Berzins, K. Kyparissoudis, R. Keating, D. G. Pellicci, Y. Hayakawa, D. I. Godfrey, and M. J. Smyth. 2005. Differential antitumor immunity mediated by NKT cell subsets in vivo. J. Exp. Med. 202: 1279-1288.
30. + invariant T-cell-receptor plus natural killer T cells in bronchial asthma. N. Engl. J. Med. 354: 1117-1129.
31. Tahir, S. M., O. Cheng, A. Shaulov, Y. Koezuka, G. J. Bubley, S. B. Wilson, S. P. Balk, and M. A. Exley. 2001. Loss of IFN-γ production by invariant NK T cells in advanced cancer. J. Immunol. 167: 4046-4050.
32. Motohashi, S., S. Kobayashi, T. Ito, K. K. Magara, O. Mikuni, N. Kamada, T. Iizasa, T. Nakayama, T. Fujisawa, and M. Taniguchi. 2002. Preserved IFN-α production of circulating Vα24 NKT cells in primary lung cancer patients. Int. J. Cancer. 102: 159-165. (Pubitemid 35168029)
33. Kawano, T., T. Nakayama, N. Kamada, Y. Kaneko, M. Harada, N. Ogura, Y. Akutsu, S. Motohashi, T. Iizasa, H. Endo, et al. 1999. Antitumor cytotoxicity mediated by ligand-activated human V α24 NKT cells. Cancer Res. 59: 5102-5105. (Pubitemid 29503967)
34. + NKT cells by age, malignancy and conventional anticancer therapies. Br. J. Cancer. 91: 1880-1886.
35. Dhodapkar, M. V., M. D. Geller, D. H. Chang, K. Shimizu, S. Fujii, K. M. Dhodapkar, and J. Krasovsky. 2003. A reversible defect in natural killer T cell function characterizes the progression of premalignant to malignant multiple myeloma. J. Exp. Med. 197: 1667-1676.
36. Dhodapkar, K. M., B. Cirignano, F. Chamian, D. Zagzag, D. C. Miller, J. L. Finlay, and R. M. Steinman. 2004. 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: 893-899.
37. Swann, J., N. Y. Crowe, Y. Hayakawa, D. I. Godfrey, and M. J. Smyth. 2004. Regulation of antitumour immunity by CD1d-restricted NKT cells. Immunol. Cell Biol. 82: 323-331. (Pubitemid 38870027)
38. Crowe, N. Y., M. J. Smyth, and D. I. Godfrey. 2002. A critical role for natural killer T cells in immunosurveillance of methylcholanthrene-induced sarcomas. J. Exp. Med. 196: 119-127. (Pubitemid 34747317)
39. Stewart, T. J., M. J. Smyth, G. J. Fernando, I. H. Frazer, and G. R. Leggatt. 2003. Inhibition of early tumor growth requires Jα18-positive (natural killer T) cells. Cancer Res. 63: 3058-3060.
40. + NK cells in vitro. J. Immunol. 165: 1659-1664.
41. 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.
42. Matsuda, J. L., O. V. Naidenko, L. Gapin, T. Nakayama, M. Taniguchi, C. R. Wang, Y. Koezuka, and M. Kronenberg. 2000. Tracking the response of natural killer T cells to a glycolipid antigen using CD1d tetramers. J. Exp. Med. 192: 741-754.
43. Exley, M. A., and M. J. Koziel. 2004. To be or not to be NKT: natural killer T cells in the liver. Hepatology 40: 1033-1040. (Pubitemid 39425556)
44. De Lalla, C., G. Galli, L. Aldrighetti, R. Romeo, M. Mariani, A. Monno, S. Nuti, M. Colombo, F. Callea, S. A. Porcelli, et al. 2004. Production of profibrotic cytokines by invariant NKT cells characterizes cirrhosis progression in chronic viral hepatitis. J. Immunol. 173: 1417-1425. (Pubitemid 38924323)
45. Kenna, T., L. Golden-Mason, S. A. Porcelli, Y. Koezuka, J. E. Hegarty, C. O'Farrelly, and D. G. Doherty. 2003. NKT cells from normal and tumor-bearing human livers are phenotypically and functionally distinct from murine NKT cells. J. Immunol. 171: 1775-1779. (Pubitemid 36969796)
46. + T cell responses in patients with hepatocellular carcinoma. J. Immunol. 174: 1709-1716.
47. Im, J. S., K. O. A. Yu, P. A. Illarionov, K. P. LeClair, J. R. Storey, M. W. Kennedy, G. S. Besra, and S. A. Porcelli. 2004. Direct measurement of antigen binding properties of CD1 proteins using fluorescent lipid probes. J. Biol. Chem. 279: 299-310.
48. + NKT cell numbers are decreased in cancer patients independent of tumor type or tumor load. Int. J. Cancer 116: 87-93.
49. Lucas, M., S. Gadola, U. Meier, N. T. Young, G. Harcourt, A. Karadimitris, N. Coumi, D. Brown, G. Dusheiko, V. Cerundolo, and P. Klenerman. 2003. Frequency and phenotype of circulating Vα24/Vβ11 double-positive natural killer T cells during hepatitis C virus infection. J. Virol. 77: 2251-2257. (Pubitemid 36110039)
50. Sandberg, J. K., N. Bhardwaj, and D. F. Nixon. 2003. Dominant effector memory characteristics, capacity for dynamic adaptive expansion, and sex bias in the innate Vα24 NKT cell compartment. Eur. J. Immunol. 33: 588-596.
51. Shimizu, Y., A. Watanabe, and T. L. Whiteside. 1992. Memory T-lymphocytes are the main population of tumor-infiltrating lymphocytes obtained from human primary liver tumors. J. Hepatol. 16: 197-202. (Pubitemid 23013198)
52. + α/β T-cells and inferior role of innate immune reaction in liver metastases. Anticancer Res. 23: 3175-3181.
53. + NKT cells activated by α-glycosylceramide-pulsed monocyte-derived dendritic cells. J. Immunol. 164: 4458-4464.
54. Wu, D. Y., N. H. Segal, S. Sidobre, M. Kronenberg, and P. B. Chapman. 2003. Cross-presentation of disialoganglioside GD3 to natural killer T cells. J. Exp. Med. 198: 173-181. (Pubitemid 36870197)
55. Blumberg, R. S., C. Terhorst, P. Bleicher, F. V. McDermott, C. H. Allan, S. B. Landau, J. S. Trier, and S. P. Balk. 1991. Expression of a nonpolymorphic MHC class I-like molecule, CD1D, by human intestinal epithelial cells. J. Immunol. 147: 2518-2524.
56. Canchis, P. W., A. K. Bhan, S. B. Landau, L. Yang, S. P. Balk, and R. S. Blumberg. 1993. Tissue distribution of the non-polymorphic major histocompatibility complex class I-like molecule, CD1d. Immunology 80: 561-565.
57. Colgan, S. P., V. M. Morales, J. L. Madara, J. E. Polischuk, S. P. Balk, and R. S. Blumberg. 1996. IFN-γ modulates CD1d surface expression on intestinal epithelia. Am. J. Physiol. 271: C276-C283. (Pubitemid 26298802)
58. Durante-Mangoni, E., R. Wang, A. Shaulov, Q. He, I. Nasser, N. Afdhal, M. J. Koziel, and M. A. Exley. 2004. Hepatic CD1d expression in hepatitis C virus infection and recognition by resident proinflammatory CD1d-reactive T cells. J. Immunol. 173: 2159-2166. (Pubitemid 38971655)
59. Cabrita, M., C. F. Pereira, P. Rodrigues, E. M. Cardoso, and F. A. Arosa. 2005. Altered expression of CD1d molecules and lipid accumulation in the human hepatoma cell line HepG2 after iron loading. FEBS J. 272: 152-165. (Pubitemid 40083075)
60. van de Wal, Y., N. Corazza, M. Allez, L. F. Mayer, H. Iijima, M. Ryan, S. Cornwall, D. Kaiserlian, R. Hershberg, Y. Koezuka, et al. 2003. Delineation of a CD1d-restricted antigen presentation pathway associated with human and mouse intestinal epithelial cells. Gastroenterology 124: 1420-1431.
61. Winau, F., G. Hegasy, R. Weiskirchen, S. Weber, C. Cassan, P. A. Sieling, R. L. Modlin, R. S. Liblau, A. M. Gressner, and S. H. Kaufmann. 2007. Ito cells are liver-resident antigen-presenting cells for activating T cell responses. Immunity 26: 117-129. (Pubitemid 46109346)
62. Yanagisawa, K., K. Seino, Y. Ishikawa, M. Nozue, T. Todoroki, and K. Fukao. 2002. Impaired proliferative response of Vα24 NKT cells from cancer patients against α-galactosylceramide. J. Immunol. 168: 6494-6499. (Pubitemid 34620075)
63. + cells producing nitric oxide. Cancer Res. 66: 11441-11446.
64. Liu, Y., R. T. Poon, J. Hughes, X. Feng, W. C. Yu, and S. T. Fan. 2005. Chemokine receptors support infiltration of lymphocyte subpopulations in human hepatocellular carcinoma. Clin. Immunol. 114: 174-182. (Pubitemid 40082383)
65. + T lymphocytes in human colorectal carcinoma. Int. J. Cancer. 116: 949-956.
66. - subsets of Vα24-invariant natural killer T cells in humans. Blood 104: 4150-4156.
67. + α-chain variable gene segment 24 (Vα24) natural killer T cells in the early human fetal thymus is regulated by IL-7. Proc. Natl. Acad. Sci. USA 101: 7058-7063.
68. Zippelius, A., P. Batard, V. Rubio-Godoy, G. Bioley, D. Lienard, F. Lejeune, D. Rimoldi, P. Guillaume, N. Meidenbauer, A. Mackensenet et al. 2004. Effector function of human tumor-specific CD8 T cells in melanoma lesions: a state of local functional tolerance. Cancer Res. 64: 2865-2873. (Pubitemid 38500627)
69. 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. (Pubitemid 35424759)
70. + NKT cells in human subjects results in highly coordinated secondary activation of acquired and innate immunity. Blood 103: 383-389.
71. 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.
72. Ishikawa, A., S. Motohashi, E. Ishikawa, H. Fuchida, K. Higashino, M. Otsuji, T. Iizasa, T. Nakayama, M. Taniguchi, and T. Fujisawa. 2005. 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: 1910-1917. (Pubitemid 40471857)
73. 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. (Pubitemid 44703772)
74. Meidenbauer, N., J. Marienhagen, M. Laumer, S. Vogl, J. Heymann, R. Andreesen, and A. Mackensen. 2003. Survival and tumor localization of adoptively transferred Melan-A-specific T cells in melanoma patients. J. Immunol. 170: 2161-2169. (Pubitemid 36197440)
75. Silk, J. D., I. F. Hermans, U. Gileadi, T. W. Chong, D. Shepherd, M. Salio, B. Mathew, R. R. Schmidt, S. J. Lunt, K. J. Williams, et al. 2004. Utilizing the adjuvant properties of CD1d-dependent NK T cells in T cell-mediated immunotherapy. J. Clin. Invest. 114: 1800-1811.
76. Schmieg, J., G. Yang, R. W. Franck, and M. Tsuji. 2003. Superior protection against malaria and melanoma metastases by a C-glycoside analogue of the natural killer T cell ligand α-galactosylceramide. J. Exp. Med. 198: 1631-1641. (Pubitemid 37494156)