Influenza virus infection augments NK cell inhibition through reorganization of major histocompatibility complex class I proteins

Journal of Virology

Volumn 82, Issue 16, 2008, Pages 8030-8037

  Achdout, Hagit ^a   Manaster, Irit ^a   Mandelboim, Ofer ^a  

^a HEBREW UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL KILLER CELL RECEPTOR; NATURAL KILLER CELL RECEPTOR KIR2DL1; NATURAL KILLER CELL RECEPTOR LIR1; NATURAL KILLER CELL RECEPTOR NKP46;

ARTICLE; CELL ACTIVITY; CELL SURFACE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXICITY; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLUENZA; INFLUENZA VIRUS; LIPID RAFT; MAJOR HISTOCOMPATIBILITY COMPLEX; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; RECEPTOR BINDING; VIRUS IMMUNITY;

ANTIBODIES, MONOCLONAL; CELL LINE, TUMOR; CELL MEMBRANE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; INFLUENZA VACCINES; INFLUENZA, HUMAN; KILLER CELLS, NATURAL; LIGANDS; MEMBRANE MICRODOMAINS; ORTHOMYXOVIRIDAE; PROTEIN BINDING; RECEPTORS, IMMUNOLOGIC; T-LYMPHOCYTES; VIRAL PROTEINS;

ORTHOMYXOVIRIDAE;

EID: 49149116128     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00870-08     Document Type: Article

References (55)

1. Achdout, H., T. I. Arnon, G. Markel, T. Gonen-Gross, G. Katz, N. Lieberman, R. Gazit, A. Joseph, E. Kedar, and O. Mandelboim. 2003. Enhanced recognition of human NK receptors after influenza virus infection. J. Immunol. 171:915-923.
2. Arnon, T. I., H. Achdout, N. Lieberman, R. Gazit, T. Gonen-Gross, G. Katz, A. Bar-Ilan, N. Bloushtain, M. Lev, A. Joseph, E. Kedar, A. Porgador, and O. Mandelboim. 2004. The mechanisms controlling the recognition of tumor- and virus-infected cells by NKp46. Blood 103:664-672.
3. Arnon, T. I., M. Lev, G. Katz, Y. Chernobrov, A. Porgador, and O. Mandelboim. 2001. Recognition of viral hemagglutinins by NKp44 but not by NKp30. Eur. J. Immunol. 31:2680-2689.
4. Arnon, T. I., G. Markel, and O. Mandelboim. 2006. Tumor and viral recognition by natural killer cells receptors. Semin. Cancer Biol. 16:348-358.
5. Baba, E., R. Erskine, J. E. Boyson, G. B. Cohen, D. M. Davis, P. Malik, O. Mandelboim, H. T. Reyburn, and J. L. Strominger. 2000. N-linked carbohydrate on human leukocyte antigen-C and recognition by natural killer cell inhibitory receptors. Hum. Immunol. 61:1202-1218.
6. Biassoni, R., C. Cantoni, D. Pende, S. Sivori, S. Parolini, M. Vitale, C. Bottino, and A. Moretta. 2001. Human natural killer cell receptors and coreceptors. Immunol. Rev. 181:203-214.
7. Bottino, C., L. Moretta, D. Pende, M. Vitale, and A. Moretta. 2004. Learning how to discriminate between friends and enemies, a lesson from natural killer cells. Mol. Immunol. 41:569-575.
8. Boyington, J. C., S. A. Motyka, P. Schuck, A. G. Brooks, and P. D. Sun. 2000. Crystal structure of an NK cell immunoglobulin-like receptor in complex with its class I MHC ligand. Nature 405:537-543.
9. Cantoni, C., C. Bottino, M. Vitale, A. Pessino, R. Augugliaro, A. Malaspina, S. Parolini, L. Moretta, A. Moretta, and R. Biassoni. 1999. NKp44, a triggering receptor involved in tumor cell lysis by activated human natural killer cells, is a novel member of the immunoglobulin superfamily. J. Exp. Med. 189:787-796.
10. Cerwenka, A., and L. L. Lanier. 2001. Natural killer cells, viruses, and cancer. Nat. Rev. Immunol. 1:41-49.
11. Chapman, T. L., A. P. Heikeman, and P. J. Bjorkman. 1999. The inhibitory receptor LIR-1 uses a common binding interaction to recognize class I MHC molecules and the viral homolog UL18. Immunity 11:603-613.
12. Cohen, G. B., R. T. Gandhi, D. M. Davis, O. Mandelboim, B. K. Chen, J. L. Strominger, and D. Baltimore. 1999. The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 10:661-671.
13. Cosman, D., N. Fanger, L. Borges, M. Kubin, W. Chin, L. Peterson, and M. L. Hsu. 1997. A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 7:273-282.
14. + T cells. J. Immunol. 166:7009-7013.
15. Fahmy, T. M., J. G. Bieler, M. Edidin, and J. P. Schneck. 2001. Increased TCR avidity after T-cell activation: a mechanism for sensing low-density antigen. Immunity 14:135-143.
16. Fan, Q. R., E. O. Long, and D. C. Wiley. 2001. Crystal structure of the human natural killer cell inhibitory receptor KIR2DL1-HLA-Cw4 complex. Nat. Immunol. 2:452-460.
17. Farrell, H. E., H. Vally, D. M. Lynch, P. Fleming, G. R. Shellam, A. A. Scalzo, and N. J. Davis-Poynter. 1997. Inhibition of natural killer cells by a cytomegalovirus MHC class I homologue in vivo. Nature 386:510-514.
18. Gazit, R., R. Gruda, M. Elboim, T. I. Arnon, G. Katz, H. Achdout, J. Hanna, U. Qimron, G. Landau, E. Greenbaum, Z. Zakay-Rones, A. Porgador, and O. Mandelboim. 2006. Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1. Nat. Immunol. 7:517-523.
19. Gubina, E., T. Chen, L. Zhang, E. F. Lizzio, and S. Kozlowski. 2002. CD43 polarization in unprimed T cells can be dissociated from raft coalescence by inhibition of HMG CoA reductase. Blood 99:2518-2525.
20. Kariko, K., D. Weissman, and F. A. Welsh. 2004. Inhibition of Toll-like receptor and cytokine signaling: a unifying theme in ischemic tolerance. J. Cereb. Blood Flow Metab. 24:1288-1304.
21. Ladasky, J. J., B. P. Shum, F. Canavez, H. N. Seuanez, and P. Parham. 1999. Residue 3 of beta2-microglobulin affects binding of class 1 MHC molecules by the W6/32 antibody. Immunogenetics 49:312-320.
22. Langlet, C., A. M. Bernard, P. Drevot, and H. T. He. 2000. Membrane rafts and signaling by the multichain immune recognition receptors. Curr. Opin. Immunol. 12:250-255.
23. Lanier, L. L. 1998. NK cell receptors. Annu. Rev. Immunol. 16:359-393.
24. Leser, G. P., and R. A. Lamb. 2005. Influenza virus assembly and budding in raft-derived microdomains: a quantitative analysis of the surface distribution of HA, NA and M2 proteins. Virology 342:215-227.
25. Long, E. O. 1999. Regulation of immune responses through inhibitory receptors. Annu. Rev. Immunol. 17:875-904.
26. Lopez-Botet, M., and T. Bellon. 1999. Natural killer cell activation and inhibition by receptors for MHC class I. Curr. Opin. Immunol. 11:301-307.
27. Mandelboim, O., S. Kent, D. M. Davis, S. B. Wilson, T. Okazaki, R. Jackson, D. Hafler, and J. L. Strominger. 1998. Natural killer activating receptors trigger interferon gamma secretion from T cells and natural killer cells. Proc. Natl. Acad. Sci. USA 95:3798-3803.
28. Mandelboim, O., N. Lieberman, M. Lev, L. Paul, T. I. Arnon, Y. Bushkin, D. M. Davis, J. L. Strominger, J. W. Yewdell, and A. Porgador. 2001. Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 409:1055-1060.
29. Mandelboim, O., P. Malik, D. M. Davis, C. H. Jo, J. E. Boyson, and J. L. Strominger. 1999. Human CD16 as a lysis receptor mediating direct natural killer cell cytotoxicity. Proc. Natl. Acad. Sci. USA 96:5640-5644.
30. Mandelboim, O., H. T. Reyburn, M. Vales-Gomez, L. Pazmany, M. Colonna, G. Borsellino, and J. L. Strominger. 1996. Protection from lysis by natural killer cells of group 1 and 2 specificity is mediated by residue 80 in human histocompatibility leukocyte antigen C alleles and also occurs with empty major histocompatibility complex molecules. J. Exp. Med. 184:913-922.
31. Markel, G., N. Lieberman, G. Katz, T. I. Arnon, M. Lotem, O. Drize, R. S. Blumberg, E. Bar-Haim, R. Mader, L. Eisenbach, and O. Mandelboim. 2002. CD66a interactions between human melanoma and NK cells: a novel class I MHC-independent inhibitory mechanism of cytotoxicity. J. Immunol. 168:2803-2810.
32. + T cells. Mol. Immunol. 42:489-494.
33. Melero, I., A. Salmeron, M. A. Balboa, J. Aramburu, and M. Lopez-Botet. 1994. Tyrosine kinase-dependent activation of human NK cell functions upon stimulation through a 58-kDa surface antigen selectively expressed on discrete subsets of NK cells and T lymphocytes. J. Immunol. 152:1662-1673.
34. Montixi, C., C. Langlet, A. M. Bernard, J. Thimonier, C. Dubois, M. A. Wurbel, J. P. Chauvin, M. Pierres, and H. T. He. 1998. Engagement of T-cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J. 17:5334-5348.
35. Moretta, A., R. Biassoni, C. Bottino, and L. Moretta. 2000. Surface receptors delivering opposite signals regulate the function of human NK cells. Semin. Immunol. 12:129-138.
36. Moretta, A., C. Bottino, M. Vitale, D. Pende, C. Cantoni, M. C. Mingari, R. Biassoni, and L. Moretta. 2001. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu. Rev. Immunol. 19:197-223.
37. Natarajan, K., N. Dimasi, J. Wang, R. A. Mariuzza, and D. H. Margulies. 2002. Structure and function of natural killer cell receptors: multiple molecular solutions to self, nonself discrimination. Annu. Rev. Immunol. 20:853-885.
38. Nayak, D. P., E. K. Hui, and S. Barman. 2004. Assembly and budding of influenza virus. Virus Res. 106:147-165.
39. Pende, D., S. Parolini, A. Pessino, S. Sivori, R. Augugliaro, L. Morelli, E. Marcenaro, L. Accame, A. Malaspina, R. Biassoni, C. Bottino, L. Moretta, and A. Moretta. 1999. Identification and molecular characterization of NKp30, a novel triggering receptor involved in natural cytotoxicity mediated by human natural killer cells. J. Exp. Med. 190:1505-1516.
40. Pessino, A., S. Sivori, C. Bottino, A. Malaspina, L. Morelli, L. Moretta, R. Biassoni, and A. Moretta. 1998. Molecular cloning of NKp46: a novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity. J. Exp. Med. 188:953-960.
41. Raulet, D. H. 2003. Roles of the NKG2D immunoreceptor and its ligands. Nat. Rev. Immunol. 3:781-790.
42. Reyburn, H. T., O. Mandelboim, M. Vales-Gomez, D. M. Davis, L. Pazmany, and J. L. Strominger. 1997. The class I MHC homologue of human cytomegalovirus inhibits attack by natural killer cells. Nature 386:514-517.
43. Rouvinski, A., I. Gahali-Sass, I. Stav, E. Metzer, H. Atlan, and A. Taraboulos. 2003. Both raft- and non-raft proteins associate with CHAPS-insoluble complexes: some APP in large complexes. Biochem. Biophys. Res. Commun. 308:750-758.
44. Scheiffele, P., A. Rietveld, T. Wilk, and K. Simons. 1999. Influenza viruses select ordered lipid domains during budding from the plasma membrane. J. Biol. Chem. 274:2038-2044.
45. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature 387:569-572.
46. Simons, K., and D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell. Biol. 1:31-39.
47. Takeda, M., G. P. Leser, C. J. Russell, and R. A. Lamb. 2003. Influenza virus hemagglutinin concentrates in lipid raft microdomains for efficient viral fusion. Proc. Natl. Acad. Sci. USA 100:14610-14617.
48. Tanabe, M., M. Sekimata, S. Ferrone, and M. Takiguchi. 1992. Structural and functional analysis of monomorphic determinants recognized by monoclonal antibodies reacting with the HLA class I alpha 3 domain. J. Immunol. 148:3202-3209.
49. Tomasec, P., V. M. Braud, C. Rickards, M. B. Powell, B. P. McSharry, S. Gadola, V. Cerundolo, L. K. Borysiewicz, A. J. McMichael, and G. W. Wilkinson. 2000. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 287:1031.
50. Ulbrecht, M., S. Martinozzi, M. Grzeschik, H. Hengel, J. W. Ellwart, M. Pla, and E. H. Weiss. 2000. Cutting edge: the human cytomegalovirus UL40 gene product contains a ligand for HLA-E and prevents NK cell-mediated lysis. J. Immunol. 164:5019-5022.
51. Willcox, B. E., G. F. Gao, J. R. Wyer, J. E. Ladbury, J. I. Bell, B. K. Jakobsen, and P. A. van der Merwe. 1999. TCR binding to peptide-MHC stabilizes a flexible recognition interface. Immunity 10:357-365.
52. Wilson, J. L., J. Charo, A. Martin-Fontecha, P. Dellabona, G. Casorati, B. J. Chambers, R. Kiessling, M. T. Bejarano, and H. G. Ljunggren. 1999. NK cell triggering by the human costimulatory molecules CD80 and CD86. J. Immunol. 163:4207-4212.
53. Yokoyama, W. M., S. Kim, and A. R. French. 2004. The dynamic life of natural killer cells. Annu. Rev. Immunol. 22:405-429.
54. Yoneda, N., E. Tatsumi, S. Kawano, K. Teshigawara, T. Oka, M. Fukuda, and N. Yamaguchi. 1992. Detection of Epstein-Barr virus genome in natural-killer-like cell line, YT. Leukemia 6:136-141.
55. Zhang, J., A. Pekosz, and R. A. Lamb. 2000. Influenza virus assembly and lipid raft microdomains: a role for the cytoplasmic tails of the spike glycoproteins. J. Virol. 74:4634-4644.