The invariant NKT cell subset in anti-viral defenses: A dark horse in anti-influenza immunity?

Journal of Leukocyte Biology

Volumn 88, Issue 4, 2010, Pages 635-643

  Kulkarni, R R ^a   Haeryfar, S M ^b   Sharif, S ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

CD1d; Glycolipids; Influenza virus; Toll like receptors; Viral immunology

Indexed keywords

GLYCOLIPID;

ADAPTIVE IMMUNITY; BACTERIAL INFECTION; CELL INTERACTION; IMMUNE RESPONSE; INFLUENZA; INFLUENZA VIRUS; INNATE IMMUNITY; NATURAL KILLER CELL; PRIORITY JOURNAL; REVIEW; VIRUS INFECTION; ANIMAL; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; NATURAL KILLER T CELL; ORTHOMYXOVIRUS; ORTHOMYXOVIRUS INFECTION;

BACTERIA (MICROORGANISMS); EQUIDAE; ORTHOMYXOVIRIDAE;

ANIMALS; HUMANS; LYMPHOCYTE ACTIVATION; NATURAL KILLER T-CELLS; ORTHOMYXOVIRIDAE; ORTHOMYXOVIRIDAE INFECTIONS; VIRUS DISEASES;

EID: 77957884099     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0410191     Document Type: Review

References (73)

1. Levitsky, H. I., Golumbek, P. T., Pardoll, D. M. (1991) The fate of CD4-8- T cell receptor-α β+ thymocytes. J. Immunol. 146, 1113-1117.
2. Makino, Y., Kanno, R., Koseki, H., Taniguchi, M. (1996) Development of Vα4+ NK T cells in the early stages of embryogenesis. Proc. Natl. Acad. Sci. USA 93, 6516-6520.
3. Yuling, H., Ruijing, X., Li, L., Xiang, J., Rui, Z., Yujuan, W., Lijun, Z., Chunxian, D., Xinti, T., Wei, X., Lang, C., Yanping, J., Tao, X., Mengjun, W., Jie, X., Youxin, J., Jinquan, T. (2009) EBV-induced human CD8+ NKT cells suppress tumorigenesis by EBV-associated malignancies. Cancer Res. 69, 7935-7944.
4. Cerundolo, V., Silk, J. D., Masri, S. H., Salio, M. (2009) Harnessing invariant NKT cells in vaccination strategies. Nat. Rev. Immunol. 9, 28-38.
5. Swain, M. G. (2008) Hepatic NKT cells: friend or foe? Clin. Sci. (Lond.) 114, 457-466.
6. Arrenberg, P., Halder, R., Kumar, V. (2009) Cross-regulation between distinct natural killer T cell subsets influences immune response to self and foreign antigens. J. Cell. Physiol. 218, 246-250.
7. Ambrosino, E., Terabe, M., Halder, R. C., Peng, J., Takaku, S., Miyake, S., Yamamura, T., Kumar, V., Berzofsky, J. A. (2007) Cross-regulation between type I and type II NKT cells in regulating tumor immunity: a new immunoregulatory axis. J. Immunol. 179, 5126-5136.
8. Halder, R. C., Aguilera, C., Maricic, I., Kumar, V. (2007) Type II NKT cell-mediated anergy induction in type I NKT cells prevents inflammatory liver disease. J. Clin. Invest. 117, 2302-2312.
9. Eberl, G., Lees, R., Smiley, S. T., Taniguchi, M., Grusby, M. J., MacDonald, H. R. (1999) Tissue-specific segregation of CD1d-dependent and CD1d-independent NK T cells. J. Immunol. 162, 6410-6419.
10. Kronenberg, M. (2005) Toward an understanding of NKT cell biology: progress and paradoxes. Annu. Rev. Immunol. 23, 877-900.
11. Sharif, S., Arreaza, G. A., Zucker, P., Mi, Q. S., Sondhi, J., Naidenko, O. V., Kronenberg, M., Koezuka, Y., Delovitch, T. L., Gombert, J. M., Leite-De-Moraes, M., Gouarin, C., Zhu, R., Hameg, A., Nakayama, T., Taniguchi, M., Lepault, F., Lehuen, A., Bach, J. F., Herbelin, A. (2001) Activation of natural killer T cells by α-galactosylceramide treatment prevents the onset and recurrence of autoimmune type 1 diabetes. Nat. Med. 7, 1057-1062.
12. Sharif, S., Arreaza, G. A., Zucker, P., Mi, Q. S., Delovitch, T. L. (2002) Regulation of autoimmune disease by natural killer T cells. J. Mol. Med. 80, 290-300.
13. Wu, L., Van Kaer, L. (2009) Natural killer T cells and autoimmune disease. Curr. Mol. Med. 9, 4-14.
14. Kinjo, Y., Kronenberg, M. (2005) V α14 iNKT cells are innate lymphocytes that participate in the immune response to diverse microbes. J. Clin. Immunol. 25, 522-533.
15. Godfrey, D. I., McCluskey, J., Rossjohn, J. (2005) CD1d antigen presentation: treats for NKT cells. Nat. Immunol. 6, 754-756.
16. Joyce, S., Woods, A. S., Yewdell, J. W., Bennink, J. R., De Silva, A. D., Boesteanu, A., Balk, S. P., Cotter, R. J., Brutkiewicz, R. R. (1998) Natural ligand of mouse CD1d1: cellular glycosylphosphatidylinositol. Science 279, 1541-1544.
17. De Silva, A. D., Park, J. J., Matsuki, N., Stanic, A. K., Brutkiewicz, R. R., Medof, M. E., Joyce, S. (2002) Lipid protein interactions: the assembly of CD1d1 with cellular phospholipids occurs in the endoplasmic reticulum. J. Immunol. 168, 723-733.
18. Zhou, D., Mattner, J., Cantu III, C., Schrantz, N., Yin, N., Gao, Y., Sagiv, Y., Hudspeth, K., Wu, Y. P., Yamashita, T., Teneberg, S., Wang, D., Proia, R. L., Levery, S. B., Savage, P. B., Teyton, L., Bendelac, A. (2004) Lysosomal glycosphingolipid recognition by NKT cells. Science 306, 1786-1789.
19. Emoto, M., Emoto, Y. (2009) Intracellular bacterial infection and invariant NKT cells. Yonsei Med. J. 50, 12-21.
20. Yu, K. O., Porcelli, S. A. (2005) The diverse functions of CD1d-restricted NKT cells and their potential for immunotherapy. Immunol. Lett. 100, 42-55.
21. Hiromatsu, T., Matsuguchi, T., Shimizu, H., Yajima, T., Nishimura, H., Arai, T., Nimura, Y., Yoshikai, Y. (2003) NK T cells stimulated with a ligand for TLR2 at least partly contribute to liver injury caused by Escherichia coli infection in mice. Eur. J. Immunol. 33, 2511-2519.
22. Shimizu, H., Matsuguchi, T., Fukuda, Y., Nakano, I., Hayakawa, T., Takeuchi, O., Akira, S., Umemura, M., Suda, T., Yoshikai, Y. (2002) Tolllike receptor 2 contributes to liver injury by Salmonella infection through Fas ligand expression on NKT cells in mice. Gastroenterology 123, 1265-1277.
23. Dong, Z., Zhang, J., Sun, R., Wei, H., Tian, Z. (2007) Impairment of liver regeneration correlates with activated hepatic NKT cells in HBV transgenic mice. Hepatology 45, 1400-1412.
24. De Lalla, C., Galli, G., Aldrighetti, L., Romeo, R., Mariani, M., Monno, A., Nuti, S., Colombo, M., Callea, F., Porcelli, S. A., Panina-Bordignon, P., Abrignani, S., Casorati, G., Dellabona, P. (2004) Production of profibrotic cytokines by invariant NKT cells characterizes cirrhosis progression in chronic viral hepatitis. J. Immunol. 173, 1417-1425.
25. Medzhitov, R. (2007) Recognition of microorganisms and activation of the immune response. Nature 449, 819-826.
26. Iwasaki, A., Medzhitov, R. (2004) Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5, 987-995.
27. Nagarajan, N. A., Kronenberg, M. (2007) Invariant NKT cells amplify the innate immune response to lipopolysaccharide. J. Immunol. 178, 2706-2713.
28. Tyznik, A. J., Tupin, E., Nagarajan, N. A., Her, M. J., Benedict, C. A., Kronenberg, M. (2008) Cutting edge: the mechanism of invariant NKT cell responses to viral danger signals. J. Immunol. 181, 4452-4456.
29. Askenase, P. W., Itakura, A., Leite-de-Moraes, M. C., Lisbonne, M., Roongapinun, S., Goldstein, D. R., Szczepanik, M. (2005) TLR-dependent IL-4 production by invariant Vα14+Jα18+ NKT cells to initiate contact sensitivity in vivo. J. Immunol. 175, 6390-6401.
30. Tupin, E., Kinjo, Y., Kronenberg, M. (2007) The unique role of natural killer T cells in the response to microorganisms. Nat. Rev. Microbiol. 5, 405-417.
31. Raftery, M. J., Winau, F., Giese, T., Kaufmann, S. H., Schaible, U. E., Schonrich, G. (2008) Viral danger signals control CD1d de novo synthesis and NKT cell activation. Eur. J. Immunol. 38, 668-679.
32. Suzuki, Y., Wakita, D., Chamoto, K., Narita, Y., Tsuji, T., Takeshima, T., Gyobu, H., Kawarada, Y., Kondo, S., Akira, S., Katoh, H., Ikeda, H., Nishimura, T. (2004) Liposome-encapsulated CpG oligodeoxynucleotides as a potent adjuvant for inducing type 1 innate immunity. Cancer Res. 64, 8754-8760.
33. Van Rhijn, I., Young, D. C., De Jong, A., Vazquez, J., Cheng, T. Y., Talekar, R., Barral, D. C., Leon, L., Brenner, M. B., Katz, J. T., Riese, R., Ruprecht, R. M., O'Connor, P. B., Costello, C. E., Porcelli, S. A., Briken, V., Moody, D. B (2009) CD1c bypasses lysosomes to present a lipopeptide antigen with 12 amino acids. J. Exp. Med. 206, 1409-1422.
34. Van Kaer, L., Joyce, S. (2006) Viral evasion of antigen presentation: not just for peptides anymore. Nat. Immunol. 7, 795-797.
35. Sanchez, D. J., Gumperz, J. E., Ganem, D. (2005) Regulation of CD1d expression and function by a herpesvirus infection. J. Clin. Invest. 115, 1369-1378.
36. Cho, S., Knox, K. S., Kohli, L. M., He, J. J., Exley, M. A., Wilson, S. B., Brutkiewicz, R. R. (2005) Impaired cell surface expression of human CD1d by the formation of an HIV-1 Nef/CD1d complex. Virology 337,242-252.
37. Kakimi, K., Guidotti, L. G., Koezuka, Y., Chisari, F. V. (2000) Natural killer T cell activation inhibits hepatitis B virus replication in vivo. J. Exp. Med. 192, 921-930.
38. Jiang, X., Shimaoka, T., Kojo, S., Harada, M., Watarai, H., Wakao, H., Ohkohchi, N., Yonehara, S., Taniguchi, M., Seino, K. (2005) Cutting edge: critical role of CXCL16/CXCR6 in NKT cell trafficking in allograft tolerance. J. Immunol. 175, 2051-2055.
39. Kakimi, K., Lane, T. E., Chisari, F. V., Guidotti, L. G. (2001) Cutting edge: inhibition of hepatitis B virus replication by activated NKT cells does not require inflammatory cell recruitment to the liver. J. Immunol. 167, 6701-6705.
40. Baron, J. L., Gardiner, L., Nishimura, S., Shinkai, K., Locksley, R., Ganem, D. (2002) Activation of a non-classical NKT cell subset in a transgenic mouse model of hepatitis B virus infection. Immunity 16, 583-594.
41. Woltman, A. M., Ter Borg, M. J., Binda, R. S., Sprengers, D., von Blomberg, B. M., Scheper, R. J., Hayashi, K., Nishi, N., Boonstra, A., van der Molen, R., Janssen, H. L. (2009) α-Galactosylceramide in chronic hepatitis B infection: results from a randomized placebo-controlled phase I/II trial. Antivir. Ther. 14, 809-818.
42. Lucas, M., Gadola, S., Meier, U., Young, N. T., Harcourt, G., Karadimitris, A., Coumi, N., Brown, D., Dusheiko, G., Cerundolo, V., Klenerman, P. (2003) Frequency and phenotype of circulating Vα24/Vβ11 doublepositive natural killer T cells during hepatitis C virus infection. J. Virol. 77, 2251-2257.
43. Yamagiwa, S., Matsuda, Y., Ichida, T., Honda, Y., Takamura, M., Sugahara, S., Ishikawa, T., Ohkoshi, S., Sato, Y., Aoyagi, Y. (2008) Sustained response to interferon-α plus ribavirin therapy for chronic hepatitis C is closely associated with increased dynamism of intrahepatic natural killer and natural killer T cells. Hepatol. Res. 38, 664-672.
44. Ohira, M., Ishiyama, K., Tanaka, Y., Doskali, M., Igarashi, Y., Tashiro, H., Hiraga, N., Imamura, M., Sakamoto, N., Asahara, T., Chayama, K., Ohdan, H. (2009) Adoptive immunotherapy with liver allograft-derived lymphocytes induces anti-HCV activity after liver transplantation in humans and humanized mice. J. Clin. Invest. 119, 3226-3235.
45. Exley, M. A., He, Q., Cheng, O., Wang, R. J., Cheney, C. P., Balk, S. P., Koziel, M. J. (2002) Cutting edge: compartmentalization of Th1-like noninvariant CD1d-reactive T cells in hepatitis C virus-infected liver. J. Immunol. 168, 1519-1523.
46. Grubor-Bauk, B., Simmons, A., Mayrhofer, G., Speck, P. G. (2003) Impaired clearance of herpes simplex virus type 1 from mice lacking CD1d or NKT cells expressing the semi-variant V α 14-J α 281 TCR. J. Immunol. 170, 1430-1434.
47. Ashkar, A. A., Rosenthal, K. L. (2003) Interleukin-15 and natural killer and NKT cells play a critical role in innate protection against genital herpes simplex virus type 2 infection. J. Virol. 77, 10168-10171.
48. Cornish, A. L., Keating, R., Kyparissoudis, K., Smyth, M. J., Carbone, F. R., Godfrey, D. I. (2006) NKT cells are not critical for HSV-1 disease resolution. Immunol. Cell Biol. 84, 13-19.
49. Exley, M. A., Bigley, N. J., Cheng, O., Shaulov, A., Tahir, S. M., Carter, Q. L., Garcia, J., Wang, C., Patten, K., Stills, H. F., Alt, F. W., Snapper, S. B., Balk, S. P. (2003) Innate immune response to encephalomyocarditis virus infection mediated by CD1d. Immunology 110, 519-526.
50. Ilyinskii, P. O., Wang, R., Balk, S. P., Exley, M. A. (2006) CD1d mediates T-cell-dependent resistance to secondary infection with encephalomyocarditis virus (EMCV) in vitro and immune response to EMCV infection in vivo. J. Virol. 80, 7146-7158.
51. Seki, S., Hashimoto, W., Ogasawara, K., Satoh, M., Watanabe, H., Habu, Y., Hiraide, H., Takeda, K. (1997) Antimetastatic effect of NK1+ T cells on experimental hematogenous tumor metastases in the liver and lungs of mice. Immunology 92, 561-566.
52. Johnson, T. R., Hong, S., Van Kaer, L., Koezuka, Y., Graham, B. S. (2002) NKT cells contribute to expansion of CD8(+) T cells and amplification of antiviral immune responses to respiratory syncytial virus. J. Virol. 76, 4294-4303.
53. Hansen, D. S., Siomos, M. A., Buckingham, L., Scalzo, A. A., Schofield, L. (2003) Regulation of murine cerebral malaria pathogenesis by CD1d-restricted NKT cells and the natural killer complex. Immunity 18, 391-402.
54. Li, D., Xu, X. N. (2008) NKT cells in HIV-1 infection. Cell Res. 18, 817-822.
55. Motsinger, A., Haas, D. W., Stanic, A. K., Van Kaer, L., Joyce, S., Unutmaz, D. (2002) CD1d-restricted human natural killer T cells are highly susceptible to human immunodeficiency virus 1 infection. J. Exp. Med. 195, 869-879.
56. Hobbs, J. A., Cho, S., Roberts, T. J., Sriram, V., Zhang, J., Xu, M., Brutkiewicz, R. R. (2001) Selective loss of natural killer T cells by apoptosis following infection with lymphocytic choriomeningitis virus. J. Virol. 75, 10746-10754.
57. Doherty, P. C., Turner, S. J., Webby, R. G., Thomas, P. G. (2006) Influenza and the challenge for immunology. Nat. Immunol. 7, 449-455.
58. Stambas, J., Guillonneau, C., Kedzierska, K., Mintern, J. D., Doherty, P. C., La Gruta, N. L. (2008) Killer T cells in influenza. Pharmacol. Ther. 120, 186-196.
59. Ho, L. P., Denney, L., Luhn, K., Teoh, D., Clelland, C., McMichael, A. J. (2008) Activation of invariant NKT cells enhances the innate immune response and improves the disease course in influenza A virus infection. Eur. J. Immunol. 38, 1913-1922.
60. Carnaud, C., Lee, D., Donnars, O., Park, S. H., Beavis, A., Koezuka, Y., Bendelac, A. (1999) Cutting edge: cross-talk between cells of the innate immune system: NKT cells rapidly activate NK cells. J. Immunol. 163, 4647-4650.
61. Benton, K. A., Misplon, J. A., Lo, C. Y., Brutkiewicz, R. R., Prasad, S. A., Epstein, S. L. (2001) Heterosubtypic immunity to influenza A virus in mice lacking IgA, all Ig, NKT cells, or γ δ T cells. J. Immunol. 166, 7437-7445.
62. De Santo, C., Salio, M., Masri, S. H., Lee, L. Y., Dong, T., Speak, A. O., Porubsky, S., Booth, S., Veerapen, N., Besra, G. S., Gröne, H. J., Platt, F. M., Zambon, M., Cerundolo, V. (2008) Invariant NKT cells reduce the immunosuppressive activity of influenza A virus-induced myeloid-derived suppressor cells in mice and humans. J. Clin. Invest. 118, 4036-4048.
63. Ko, S. Y., Ko, H. J., Chang, W. S., Park, S. H., Kweon, M. N., Kang, C. Y. (2005) α-Galactosylceramide can act as a nasal vaccine adjuvant inducing protective immune responses against viral infection and tumor. J. Immunol. 175, 3309-3317.
64. Youn, H. J., Ko, S. Y., Lee, K. A., Ko, H. J., Lee, Y. S., Fujihashi, K., Boyaka, P. N., Kim, S. H., Horimoto, T., Kweon, M. N., Kang, C. Y. (2007) A single intranasal immunization with inactivated influenza virus and α-galactosylceramide induces long-term protective immunity without redirecting antigen to the central nervous system. Vaccine 25, 5189-5198.
65. Stober, D., Jomantaite, I., Schirmbeck, R., Reimann, J. (2003) NKT cells provide help for dendritic cell-dependent priming of MHC class I-restricted CD8+ T cells in vivo. J. Immunol. 170, 2540-2548.
66. Galli, G., Pittoni, P., Tonti, E., Malzone, C., Uematsu, Y., Tortoli, M., Maione, D., Volpini, G., Finco, O., Nuti, S., Tavarini, S., Dellabona, P., Rappuoli, R., Casorati, G., Abrignani, S. (2007) Invariant NKT cells sustain specific B cell responses and memory. Proc. Natl. Acad. Sci. USA 104, 3984-3989.
67. Guillonneau, C., Mintern, J. D., Hubert, F. X., Hurt, A. C., Besra, G. S., Porcelli, S., Barr, I. G., Doherty, P. C., Godfrey, D. I., Turner, S. J. (2009) Combined NKT cell activation and influenza virus vaccination boosts memory CTL generation and protective immunity. Proc. Natl. Acad. Sci. USA 106, 3330-3335.
68. Singh, N., Hong, S., Scherer, D. C., Serizawa, I., Burdin, N., Kronenberg, M., Koezuka, Y., Van Kaer, L. (1999) Cutting edge: activation of NK T cells by CD1d and α-galactosylceramide directs conventional T cells to the acquisition of a Th2 phenotype. J. Immunol. 163, 2373-2377.
69. Miyamoto, K., Miyake, S., Yamamura, T. (2001) A synthetic glycolipid prevents autoimmune encephalomyelitis by inducing TH2 bias of natural killer T cells. Nature 413, 531-534.
70. Haeryfar, S. M., Lan, Z., Leon-Ponte, M., Duffy, K. R., Ge, W., Liu, W., Mele, T., Garcia, B., Wang, H. (2008) Prolongation of cardiac allograft survival by rapamycin and the invariant natural killer T cell glycolipid agonist OCH. Transplantation 86, 460-468.
71. Yu, K. O., Im, J. S., Molano, A., Dutronc, Y., Illarionov, P. A., Forestier, C., Fujiwara, N., Arias, I., Miyake, S., Yamamura, T., Chang, Y. T., Besra, G. S., Porcelli, S. A. (2005) Modulation of CD1d-restricted NKT cell responses by using N-acyl variants of α-galactosylceramides. Proc. Natl. Acad. Sci. USA 102, 3383-3388.
72. Kopecky-Bromberg, S. A., Fraser, K. A., Pica, N., Carnero, E., Moran, T. M., Franck, R. W., Tsuji, M., Palese, P. (2009) α-C-galactosylceramide as an adjuvant for a live attenuated influenza virus vaccine. Vaccine 27, 3766-3774.
73. Schmieg, J., Yang, G., Franck, R. W., Tsuji, M. (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.