Pivotal advance: Invariant NKT cells reduce accumulation of inflammatory monocytes in the lungs and decrease immune-pathology during severe influenza A virus infection

Journal of Leukocyte Biology

Volumn 91, Issue 3, 2012, Pages 357-368

  Kok, Wai Ling ^a   Denney, Laura ^a   Benam, Kambez ^a   Cole, Suzanne ^a   Clelland, Colin ^b   McMichael, Andrew J ^a   Ho, Ling Pei ^a,c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^c CHURCHILL HOSPITAL   (United Kingdom)

Author keywords

Chemokines; iNKT; Innate immune response; Lung injury; Respiratory viruses

Indexed keywords

CD1D ANTIGEN; MONOCYTE CHEMOTACTIC PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; DISEASE SEVERITY; INFLUENZA A; INNATE IMMUNITY; LUNG INJURY; MONOCYTE; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTIBODIES, BLOCKING; ANTIGENS, CD1D; ANTIGENS, LY; CHEMOKINE CCL2; HUMANS; IMMUNOPHENOTYPING; INFLAMMATION; INFLUENZA A VIRUS; LUNG; LYMPHOCYTE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOCYTES; NATURAL KILLER T-CELLS; ORTHOMYXOVIRIDAE INFECTIONS; RESPIRATORY MUCOSA;

INFLUENZA A VIRUS; MUS;

EID: 84857880036     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0411184     Document Type: Article

References (39)

1. De Jong, M.D., Simmons, C.P., Thanh, T.T., Hien, V.M., Smith, G.J., Chau, T.N., Hoang, D.M., Chau, N.V., Khanh, T.H., Dong, V.C., Qui, P.T., Cam, B.V., Ha do, Q., Guan, Y., Peiris, J. S., Chinh, N. T., Hien, T. T., Farrar, J. (2006) Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat. Med. 12, 1203-1207.
2. Kash, J. C., Tumpey, T. M., Proll, S. C., Carter, V., Perwitasari, O., Thomas, M. J., Basler, C. F., Palese, P., Taubenberger, J. K., García-Sastre, A., Swayne, D. E., Katze, M. G. (2006) Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. Nature 443, 578-581.
3. McGill, J., Heusel, J. W., Legge, K. L. (2009) Innate immune control and regulation of influenza virus infections. J. Leukoc. Biol. 86, 803-812.
4. Tumpey, T. M., García-Sastre, A., Taubenberger, J. K., Palese, P., Swayne, D. E., Pantin-Jackwood, M. J., Schultz-Cherry, S., Solórzano, A., Van Rooijen, N., Katz, J. M., Basler, C. F. (2005) Pathogenicity of influenza viruses with genes from the 1918 pandemic virus: functional roles of alveolar macrophages and neutrophils in limiting virus replication and. mortality in mice. J. Virol. 79, 14933-14944.
5. Dessing, M. C., van der Sluijs, K. F., Florquin, S., van der Poll, T. (2007) Monocyte chemoattractant protein 1 contributes to an adequate immune response in influenza pneumonia. Clin. Immunol. 125, 328-336.
6. Jayasekera, J. P., Vinuesa, C. G., Karupiah, G., King, N. J. (2006) Enhanced antiviral antibody secretion and attenuated immunopathology during influenza virus infection in nitric oxide synthase-2-deficient mice. J. Gen. Virol. 87, 3361-3371.
7. Dawson, T. C., Beck, M. A., Kuziel, W. A., Henderson, F., Maeda, N. (2000) Contrasting effects of CCR5 and CCR2 deficiency in the pulmonary inflammatory response to influenza A virus. Am. J. Pathol. 156, 1951-1959.
8. Godfrey, D. I., Stankovic, S., Baxter, A. G. (2010) Raising the NKT cell family. Nat. Immunol. 11, 197-206.
9. Brigl, M., Bry, L., Kent, S. C., Gumperz, J. E., Brenner, M. B. (2003) Mechanism of CD1d restricted natural killer T cell activation during microbial infection. Nat. Immunol. 4, 1230-1237.
10. Van Dommelen, S. L., Degli-Esposti, M. A. (2004) NKT cells and viral immunity. Immunol. Cell Biol. 82, 332-341.
11. 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.
12. Kamijuku, H., Nagata, Y., Jiang, X., Ichinohe, T., Tashiro, T., Mori, K., Taniguchi, M., Hase, K., Ohno, H., Shimaoka, T., Yonehara, S., Odagiri, T., Tashiro, M., Sata, T., Hasegawa, H., Seino, K. I. (2008) Mechanism of NKT cell activation by intranasal coadministration of _-galactosylceramide, which can induce cross-protection against influenza viruses. Mucosal Immunol. 1, 208-218.
13. Diana, J., Lehuen, A. (2009) NKT cells: friend or foe during viral infections? Eur. J. Immunol. 39, 3283-3291.
14. Cohen, N. R., Garg, S., Brenner, M. B. (2009) Antigen presentation by CD1 lipids, T cells, and NKT cells in microbial immunity. Adv. Immunol. 102, 1-94.
15. Lin, Y., Roberts, T. J., Spence, P. M., Brutkiewicz, R. R. (2005) Reduction in CD1d expression on dendritic cells and macrophages by an acute virus infection. J. Leukoc. Biol. 77, 151-158.
16. Yuan, W., Dasgupta, A., Cresswell, P. (2006) Herpes simplex virus evades natural killer T cell recognition by suppressing CD1d recycling. Nat. Immunol. 7, 835-842.
17. 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.
18. 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.
19. Cui, J., Shin, T., Kawano, T., Sato, H., Kondo, E., Toura, I., Kaneko, Y., Koseki, H., Kanno, M., Taniguchi, M. (1997) Requirement for Vα14 NKT cells in IL-12-mediated rejection of tumors. Science 278, 1623-1626.
20. Moskophidis, D., Kioussis, D. (1998) Contribution of virus-specific CD8+ cytotoxic T cells to virus clearance or pathologic manifestations of influenza virus infection in a T cell receptor transgenic mouse model. J. Exp. Med. 188, 223-232.
21. Ho, L. P., Urban, B. C., Jones, L., Ogg, G. S., McMichael, A. J. (2004) CD4(-) CD8aa subset of CD1d-restricted NKT cells controls T cell expansion. J. Immunol. 172, 7350-7358.
22. Geissmann, F., Jung, S., Littman, D. R. (2003) Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19, 71-82.
23. Serbina, N. V., Salazar-Mather, T. P., Biron, C. A., Kuziel, W. A., Pamer, E. G. (2003) TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19, 59-70.
24. Dai, X. M., Ryan, G. R., Hapel, A. J., Dominguez, M. G., Russell, R. G., Kapp, S., Sylvestre, V., Stanley, E. R. (2002) Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood 99, 111-120.
25. Serbina, N. V., Jia, T., Hohl, T. M., Pamer, E. G. (2008) Monocyte-mediated defense against microbial pathogens. Annu. Rev. Immunol. 26, 421-452.
26. Aldridge, J. R., Moseley, C. E., Boltz, D. A., Negovetich, N. J., Reynolds, C., Franks, J., Brown, S. A., Doherty, P. C., Webster, R. G., Thomas, P. G. (2009) TNF/iNOS-producing dendritic cells are the necessary evil of lethal influenza virus infection. Proc. Natl. Acad. Sci. USA 106, 5306-5311.
27. Auffray, C., Sieweke, M. H., Geissmann, F. (2009) Blood monocytes: development, heterogeneity and relationship with dendritic cells. Annu. Rev. Immunol. 27, 669-692.
28. Auffray, C., Fogg, D. K., Narni-Mancinelli, E., Senechal, B., Trouillet, C., Saederup, N., Leemput, J., Bigot, K., Campisi, L., Abitbol, M., Molina, T., Charo, I., Hume, D. A., Cumano, A., Lauvau, G., Geissmann, F. (2009) CX3CR1+CD115+CD135+ common macrophage/DC precursors and the role of CX3CR1 in their response to inflammation. J. Exp. Med. 206, 595-606.
29. Egan, C. E., Sukhumavasi, W., Bierly, A. L., Denkers, E. Y. (2008) Understanding the multiple functions of Gr-1(+) cell subpopulations during microbial infection. Immunol. Res. 40, 35-48.
30. Gordon, S., Taylor, P. R. (2005) Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5, 953-964.
31. Paget, C., Ivanov, S., Fontaine, J., Blanc, F., Pichavant, M., Renneson, J., Bialecki, E., Pothlichet, J., Vendeville, C., Barba-Speath, G., Huerre, M. R., Faveeuw, C., Si-Tahar, M., Trottein, F. (2011) Potential role of invariant NKT cells in the control of pulmonary inflammation and CD8+ T cell response during acute influenza A virus H3N2 pneumonia. J. Immunol. 186, 5590-5602.
32. Yadav, A., Saini, V., Arora, S. (2010) MCP-1: chemoattractant with a role beyond immunity: a review. Clin. Chim. Acta 411, 1570-1579.
33. Valente, A. J., Xie, J. F., Abramova, M. A., Wenzel, U. O., Abboud, H. E., Graves, D. T. (1998) A complex element regulates IFN-stimulated monocyte chemoattractant protein-1 gene transcription. J. Immunol. 161, 3719-3728.
34. Song, L., Asgharzadeh, S., Salo, J., Engell, K., Wu, H. W., Sposto, R., Ara, T., Silverman, A. M., DeClerck, Y. A., Seeger, R. C., Metelitsa, L. S. (2009) Vα24-invariant NKT cells mediate antitumor activity via killing of tumor-associated macrophages. J. Clin. Invest. 119, 1524-1536.
35. Yang, O. O., Racke, F. K., Nguyen, P. T., Gausling, R., Severino, M. E., Horton, H. F., Byrne, M. C., Strominger, J. L., Wilson, S. B. (2000) CD1d on myeloid dendritic cells stimulates cytokine secretion from and cytolytic activity of V α 24J α Q T cells: a feedback mechanism for immune regulation. J. Immunol. 165, 3756-3762.
36. Brigl, M., Brenner, M. B. (2010) How invariant natural killer T cells respond to infection by recognizing microbial or endogenous lipid antigens. Semin. Immunol. 22, 79-86.
37. Leite-De-Moraes, M. C., Hameg, A., Arnould, A., Machavoine, F., Koezuka, Y., Schneider, E., Herbelin, A., Dy, M. (1999) A distinct IL-18-induced pathway to fully activate NK T lymphocytes independently from TCR engagement. J. Immunol. 163, 5871-5876.
38. Gumperz, J. E., Miyake, S., Yamamura, T., Brenner, M. B. (2002) Functionally distinct subsets of CD1d-restricted natural killer T cells revealed by CD1d tetramer staining. J. Exp. Med. 195, 625-636.
39. De Santo, C., Arscott, R., Booth, S., Karydis, I., Jones, M., Asher, R., Salio, M., Middleton, M., Cerundolo, V. (2010) Invariant NKT cells modulate the suppressive activity of IL-10-secreting neutrophils differentiated with serum amyloid A. Nat. Immunol. 11, 1039-1046.