Advertisement

Virus Interactions with NK Cell Receptors

  • Vanda Juranić Lisnić
  • Iva Gašparović
  • Astrid Krmpotić
  • Stipan JonjićEmail author
Chapter

Abstract

Natural killer cells are among the first cells of the immune response to recognize and react to threats. They do so by surveying other cells for aberrant behavior such as altered expression of MHC class I, and molecules produced or induced by pathogens. As such, they are very important in host resistance to viral infection. Various unrelated viruses have evolved numerous evasion techniques in order to avoid detection by NK cells. The many immunoevasive techniques may be roughly divided into two main groups: camouflage of infected cells aimed at inhibitory receptors and obstruction of activating receptors. By differential downmodulation of MHC class I molecules and production of MHC class I homologues, viruses prevent CTL recognition and camouflage their presence from NK cells. Additionally, viruses have directed even greater attention towards preventing the engagement of activating receptors by interfering with the receptors per se or by down modulating their ligands and coactivating molecules, providing soluble competitors, modification and interference with translation of ligands.

Keywords

Natural Killer Natural Killer Cell Natural Killer Cell Cytotoxicity NKG2D Ligand Natural Killer Cell Receptor 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Kirwan SE, Burshtyn DN (2007) Regulation of natural killer cell activity. Curr Opin Immunol 19(1):46–54PubMedCrossRefGoogle Scholar
  2. 2.
    Karre K et al (1986) Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 319(6055):675–678PubMedCrossRefGoogle Scholar
  3. 3.
    Valiante NM et al (1997) Killer cell receptors: keeping pace with MHC class I evolution. Immunol Rev 155:155–164PubMedCrossRefGoogle Scholar
  4. 4.
    Raulet DH et al (1997) Specificity, tolerance and developmental regulation of natural killer cells defined by expression of class I-specific Ly49 receptors. Immunol Rev 155:41–52PubMedCrossRefGoogle Scholar
  5. 5.
    Yokoyama WM, Kim S (2006) How do natural killer cells find self to achieve tolerance? Immunity 24(3):249–257PubMedCrossRefGoogle Scholar
  6. 6.
    Kim S et al (2005) Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 436(7051):709–713PubMedCrossRefGoogle Scholar
  7. 7.
    Raulet DH, Vance RE (2006) Self-tolerance of natural killer cells. Nat Rev Immunol 6(7):520–531PubMedCrossRefGoogle Scholar
  8. 8.
    Fernandez NC et al (2005) A subset of natural killer cells achieves self-tolerance without expressing inhibitory receptors specific for self-MHC molecules. Blood 105(11):4416–4423PubMedCrossRefGoogle Scholar
  9. 9.
    Lanier LL (2003) Natural killer cell receptor signaling. Curr Opin Immunol 15(3):308–314PubMedCrossRefGoogle Scholar
  10. 10.
    Lanier LL (2008) Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol 9(5):495–502PubMedCrossRefGoogle Scholar
  11. 11.
    Raulet DH (2003) Natural killer cells. In: Paul WE (ed) Fundamental immunology. Lippincott Williams & Wilkins, Philadelphia, pp 365–391Google Scholar
  12. 12.
    Dimasi N, Biassoni R (2005) Structural and functional aspects of the Ly49 natural killer cell receptors. Immunol Cell Biol 83(1):1–8PubMedCrossRefGoogle Scholar
  13. 13.
    Dimasi N, Moretta L, Biassoni R (2004) Structure of the Ly49 family of natural killer (NK) cell receptors and their interaction with MHC class I molecules. Immunol Res 30(1):95–104PubMedCrossRefGoogle Scholar
  14. 14.
    Daniels KA et al (2001) Murine cytomegalovirus is regulated by a discrete subset of natural killer cells reactive with monoclonal antibody to Ly49H. J Exp Med 194(1):29–44PubMedCrossRefGoogle Scholar
  15. 15.
    Smith HR et al (2002) Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc Natl Acad Sci USA 99(13):8826–8831PubMedGoogle Scholar
  16. 16.
    Lee SH et al (2001) Susceptibility to mouse cytomegalovirus is associated with deletion of an activating natural killer cell receptor of the C-type lectin superfamily. Nat Genet 28(1):42–45PubMedCrossRefGoogle Scholar
  17. 17.
    Brown MG et al (2001) Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science 292(5518):934–937PubMedCrossRefGoogle Scholar
  18. 18.
    Arase H et al (2002) Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296(5571):1323–1326PubMedCrossRefGoogle Scholar
  19. 19.
    Adams EJ et al (2007) Structural elucidation of the m157 mouse cytomegalovirus ligand for Ly49 natural killer cell receptors. Proc Natl Acad Sci USA 104(24):10128–10133PubMedCrossRefGoogle Scholar
  20. 20.
    Bubic I et al (2004) Gain of virulence caused by loss of a gene in murine cytomegalovirus. J Virol 78(14):7536–7544PubMedCrossRefGoogle Scholar
  21. 21.
    Kielczewska, A., et al. (2009) Ly49P recognition of cytomegalovirus-infected cells expressing H2-Dk and the virally encoded glycoprotein m04 is associated with NK cell-mediated resistance to infection. J Exp Med 206(3):515–523Google Scholar
  22. 22.
    Ortaldo JR, Young HA (2005) Mouse Ly49 NK receptors: balancing activation and inhibition. Mol Immunol 42(4):445–450PubMedCrossRefGoogle Scholar
  23. 23.
    Trowsdale J et al (2001) The genomic context of natural killer receptor extended gene families. Immunol Rev 181:20–38PubMedCrossRefGoogle Scholar
  24. 24.
    Vilches C, Parham P (2002) KIR: diverse, rapidly evolving receptors of innate and adaptive immunity. Annu Rev Immunol 20:217–251PubMedCrossRefGoogle Scholar
  25. 25.
    Boyington JC, Sun PD (2002) A structural perspective on MHC class I recognition by killer cell immunoglobulin-like receptors. Mol Immunol 38(14):1007–1021PubMedCrossRefGoogle Scholar
  26. 26.
    Colonna M et al (1999) A novel family of Ig-like receptors for HLA class I molecules that modulate function of lymphoid and myeloid cells. J Leukoc Biol 66(3):375–381PubMedGoogle Scholar
  27. 27.
    Colonna M et al (1997) A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J Exp Med 186(11):1809–1818PubMedCrossRefGoogle Scholar
  28. 28.
    Cosman D et al (1997) A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 7(2):273–282PubMedCrossRefGoogle Scholar
  29. 29.
    Vitale M et al (1999) The leukocyte Ig-like receptor (LIR)-1 for the cytomegalovirus UL18 protein displays a broad specificity for different HLA class I alleles: analysis of LIR-1 + NK cell clones. Int Immunol 11(1):29–35PubMedCrossRefGoogle Scholar
  30. 30.
    Lepin EJ et al (2000) Functional characterization of HLA-F and binding of HLA-F tetramers to ILT2 and ILT4 receptors. Eur J Immunol 30(12):3552–3561PubMedCrossRefGoogle Scholar
  31. 31.
    Yokoyama WM, Plougastel BF (2003) Immune functions encoded by the natural killer gene complex. Nat Rev Immunol 3(4):304–316PubMedCrossRefGoogle Scholar
  32. 32.
    Raulet DH (2003) Roles of the NKG2D immunoreceptor and its ligands. Nat Rev Immunol 3(10):781–790PubMedCrossRefGoogle Scholar
  33. 33.
    Diefenbach A et al (2002) Selective associations with signaling proteins determine stimulatory versus costimulatory activity of NKG2D. Nat Immunol 3(12):1142–1149PubMedCrossRefGoogle Scholar
  34. 34.
    Mistry AR, O'Callaghan CA (2007) Regulation of ligands for the activating receptor NKG2D. Immunology 121(4):439–447PubMedCrossRefGoogle Scholar
  35. 35.
    Eagle RA, Trowsdale J (2007) Promiscuity and the single receptor: NKG2D. Nat Rev Immunol 7(9):737–744PubMedCrossRefGoogle Scholar
  36. 36.
    Cerwenka A et al (2000) Retinoic acid early inducible genes define a ligand family for the activating NKG2D receptor in mice. Immunity 12(6):721–727PubMedCrossRefGoogle Scholar
  37. 37.
    Girardi M et al (2001) Regulation of cutaneous malignancy by gammadelta T cells. Science 294(5542):605–609PubMedCrossRefGoogle Scholar
  38. 38.
    Carayannopoulos LN et al (2002) Ligands for murine NKG2D display heterogeneous binding behavior. Eur J Immunol 32(3):597–605PubMedCrossRefGoogle Scholar
  39. 39.
    Takada A et al (2008) Two novel NKG2D ligands of the mouse H60 family with differential expression patterns and binding affinities to NKG2D. J Immunol 180(3):1678–1685PubMedGoogle Scholar
  40. 40.
    Diefenbach A et al (2000) Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nat Immunol 1(2):119–126PubMedCrossRefGoogle Scholar
  41. 41.
    Carayannopoulos LN et al (2002) Cutting edge: murine UL16-binding protein-like transcript 1: a newly described transcript encoding a high-affinity ligand for murine NKG2D. J Immunol 169(8):4079–4083PubMedGoogle Scholar
  42. 42.
    Ogasawara K, Lanier LL (2005) NKG2D in NK and T cell-mediated immunity. J Clin Immunol 25(6):534–540PubMedCrossRefGoogle Scholar
  43. 43.
    Giorda R et al (1990) NKR-P1, a signal transduction molecule on natural killer cells. Science 249(4974):1298–1300PubMedCrossRefGoogle Scholar
  44. 44.
    Giorda R, Trucco M (1991) Mouse NKR-P1: a family of genes selectively coexpressed in adherent lymphokine-activated killer cells. J Immunol 147(5):1701–1708PubMedGoogle Scholar
  45. 45.
    Mesci A et al (2006) NKR-P1 biology: from prototype to missing self. Immunol Res 35(1–2):13–26PubMedCrossRefGoogle Scholar
  46. 46.
    Walzer T et al (2007) Identification, activation, and selective in vivo ablation of mouse NK cells via NKp46. Proc Natl Acad Sci U S A 104(9):3384–3389PubMedCrossRefGoogle Scholar
  47. 47.
    Gazit R et al (2006) Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1. Nat Immunol 7(5):517–523PubMedCrossRefGoogle Scholar
  48. 48.
    Bottino C et al (2000) The human natural cytotoxicity receptors (NCR) that induce HLA class I-independent NK cell triggering. Hum Immunol 61(1):1–6PubMedCrossRefGoogle Scholar
  49. 49.
    Hollyoake M, Campbell RD, Aguado B (2005) NKp30 (NCR3) is a pseudogene in 12 inbred and wild mouse strains, but an expressed gene in Mus caroli. Mol Biol Evol 22(8):1661–1672PubMedCrossRefGoogle Scholar
  50. 50.
    Biassoni R et al (2003) Human natural killer cell receptors: insights into their molecular function and structure. J Cell Mol Med 7(4):376–387PubMedCrossRefGoogle Scholar
  51. 51.
    Mandelboim O et al (2001) Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 409(6823):1055–1060PubMedCrossRefGoogle Scholar
  52. 52.
    Arnon TI et al (2001) Recognition of viral hemagglutinins by NKp44 but not by NKp30. Eur J Immunol 31(9):2680–2689PubMedCrossRefGoogle Scholar
  53. 53.
    Moretta A et al (2001) Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol 19:197–223PubMedCrossRefGoogle Scholar
  54. 54.
    Nattermann J et al (2006) Surface expression and cytolytic function of natural killer cell receptors is altered in chronic hepatitis C. Gut 55(6):869–877PubMedCrossRefGoogle Scholar
  55. 55.
    De Maria A et al (2003) The impaired NK cell cytolytic function in viremic HIV-1 infection is associated with a reduced surface expression of natural cytotoxicity receptors (NKp46, NKp30 and NKp44). Eur J Immunol 33(9):2410–2418PubMedCrossRefGoogle Scholar
  56. 56.
    Alcami A, Koszinowski UH (2000) Viral mechanisms of immune evasion. Immunol Today 21(9):447–455PubMedCrossRefGoogle Scholar
  57. 57.
    Farrell HE et al (2002) Function of CMV-encoded MHC class I homologues. Curr Top Microbiol Immunol 269:131–151PubMedGoogle Scholar
  58. 58.
    Chapman TL, Bjorkman PJ (1998) Characterization of a murine cytomegalovirus class I major histocompatibility complex (MHC) homolog: comparison to MHC molecules and to the human cytomegalovirus MHC homolog. J Virol 72(1):460–466PubMedGoogle Scholar
  59. 59.
    Browne H et al (1990) A complex between the MHC class I homologue encoded by human cytomegalovirus and beta 2 microglobulin. Nature 347(6295):770–772PubMedCrossRefGoogle Scholar
  60. 60.
    Fahnestock ML et al (1995) The MHC class I homolog encoded by human cytomegalovirus binds endogenous peptides. Immunity 3(5):583–590PubMedCrossRefGoogle Scholar
  61. 61.
    Reyburn HT et al (1997) The class I MHC homologue of human cytomegalovirus inhibits attack by natural killer cells. Nature 386(6624):514–517PubMedCrossRefGoogle Scholar
  62. 62.
    Willcox BE, Thomas LM, Bjorkman PJ (2003) Crystal structure of HLA-A2 bound to LIR-1, a host and viral major histocompatibility complex receptor. Nat Immunol 4(9):913–919PubMedCrossRefGoogle Scholar
  63. 63.
    Rudd PM et al (2001) Glycosylation and the immune system. Science 291(5512):2370–2376PubMedCrossRefGoogle Scholar
  64. 64.
    Park B et al (2002) The MHC class I homolog of human cytomegalovirus is resistant to down-regulation mediated by the unique short region protein (US)2, US3, US6, and US11 gene products. J Immunol 168(7):3464–3469PubMedGoogle Scholar
  65. 65.
    Lin A, Xu H, Yan W (2007) Modulation of HLA expression in human cytomegalovirus immune evasion. Cell Mol Immunol 4(2):91–98PubMedGoogle Scholar
  66. 66.
    Kim Y et al (2008) Human cytomegalovirus UL18 utilizes US6 for evading the NK and T-cell responses. PLoS Pathog 4(8):e1000123CrossRefGoogle Scholar
  67. 67.
    Leong CC et al (1998) Modulation of natural killer cell cytotoxicity in human cytomegalovirus infection: the role of endogenous class I major histocompatibility complex and a viral class I homolog. J Exp Med 187(10):1681–1687PubMedCrossRefGoogle Scholar
  68. 68.
    ProD'homme V et al (2007) The human cytomegalovirus MHC class I homolog UL18 inhibits LIR-1+ but activates LIR-1- NK cells. J Immunol 178(7):4473–4481PubMedGoogle Scholar
  69. 69.
    Natarajan K et al (2006) Crystal structure of the murine cytomegalovirus MHC-I homolog m144. J Mol Biol 358(1):157–171PubMedCrossRefGoogle Scholar
  70. 70.
    Farrell HE et al (1997) Inhibition of natural killer cells by a cytomegalovirus MHC class I homologue in vivo. Nature 386(6624):510–514PubMedCrossRefGoogle Scholar
  71. 71.
    Beisser PS et al (2000) The r144 major histocompatibility complex class I-like gene of rat cytomegalovirus is dispensable for both acute and long-term infection in the immunocompromised host. J Virol 74(2):1045–1050PubMedCrossRefGoogle Scholar
  72. 72.
    Senkevich TG et al (1996) Genome sequence of a human tumorigenic poxvirus: prediction of specific host response-evasion genes. Science 273(5276):813–816PubMedCrossRefGoogle Scholar
  73. 73.
    Tomasec P et al (2000) Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 287(5455):1031PubMedCrossRefGoogle Scholar
  74. 74.
    Ulbrecht M et al (2000) Cutting edge: the human cytomegalovirus UL40 gene product contains a ligand for HLA-E and prevents NK cell-mediated lysis. J Immunol 164(10):5019–5022PubMedGoogle Scholar
  75. 75.
    Ziegler H et al (1997) A mouse cytomegalovirus glycoprotein retains MHC class I complexes in the ERGIC/cis-Golgi compartments. Immunity 6(1):57–66PubMedCrossRefGoogle Scholar
  76. 76.
    Reusch U et al (1999) A cytomegalovirus glycoprotein re-routes MHC class I complexes to lysosomes for degradation. EMBO J 18(4):1081–1091PubMedCrossRefGoogle Scholar
  77. 77.
    Kavanagh DG, Koszinowski UH, Hill AB (2001) The murine cytomegalovirus immune evasion protein m4/gp34 forms biochemically distinct complexes with class I MHC at the cell surface and in a pre-Golgi compartment. J Immunol 167(7):3894–3902PubMedGoogle Scholar
  78. 78.
    Kleijnen MF et al (1997) A mouse cytomegalovirus glycoprotein, gp34, forms a complex with folded class I MHC molecules in the ER which is not retained but is transported to the cell surface. EMBO J 16(4):685–694PubMedCrossRefGoogle Scholar
  79. 79.
    Pinto AK et al (2006) Coordinated function of murine cytomegalovirus genes completely inhibits CTL lysis. J Immunol 177(5):3225–3234PubMedGoogle Scholar
  80. 80.
    Holtappels R et al (2006) Cytomegalovirus encodes a positive regulator of antigen presentation. J Virol 80(15):7613–7624PubMedCrossRefGoogle Scholar
  81. 81.
    Nattermann J et al (2005) HIV-1 infection leads to increased HLA-E expression resulting in impaired function of natural killer cells. Antivir Ther 10(1):95–107PubMedGoogle Scholar
  82. 82.
    Martini F et al (2005) HLA-E up-regulation induced by HIV infection may directly contribute to CD94-mediated impairment of NK cells. Int J Immunopathol Pharmacol 18(2):269–276PubMedGoogle Scholar
  83. 83.
    Cohen GB et al (1999) The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 10(6):661–671PubMedCrossRefGoogle Scholar
  84. 84.
    Ishido S et al (2000) Downregulation of major histocompatibility complex class I molecules by Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins. J Virol 74(11):5300–5309PubMedCrossRefGoogle Scholar
  85. 85.
    Ishido S et al (2000) Inhibition of natural killer cell-mediated cytotoxicity by Kaposi's sarcoma-associated herpesvirus K5 protein. Immunity 13(3):365–374PubMedCrossRefGoogle Scholar
  86. 86.
    Guma M et al (2004) Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood 104(12):3664–3671PubMedCrossRefGoogle Scholar
  87. 87.
    Guma M et al (2006) Human cytomegalovirus infection is associated with increased proportions of NK cells that express the CD94/NKG2C receptor in aviremic HIV-1-positive patients. J Infect Dis 194(1):38–41PubMedCrossRefGoogle Scholar
  88. 88.
    Guma M et al (2006) Expansion of CD94/NKG2C+ NK cells in response to human cytomegalovirus-infected fibroblasts. Blood 107(9):3624–3631PubMedCrossRefGoogle Scholar
  89. 89.
    Carlyle JR et al (2004) Missing self-recognition of Ocil/Clr-b by inhibitory NKR-P1 natural killer cell receptors. Proc Natl Acad Sci USA 101(10):3527–3532PubMedCrossRefGoogle Scholar
  90. 90.
    Voigt S et al (2007) Cytomegalovirus evasion of innate immunity by subversion of the NKR-P1B:Clr-b missing-self axis. Immunity 26(5):617–627PubMedCrossRefGoogle Scholar
  91. 91.
    Meier UC et al (2005) Shared alterations in NK cell frequency, phenotype, and function in chronic human immunodeficiency virus and hepatitis C virus infections. J Virol 79(19):12365–12374PubMedCrossRefGoogle Scholar
  92. 92.
    Titanji K et al (2008) Altered distribution of natural killer cell subsets identified by CD56, CD27 and CD70 in primary and chronic human immunodeficiency virus-1 infection. Immunology 123(2):164–170PubMedGoogle Scholar
  93. 93.
    O'Connor GM et al (2007) Natural Killer cells from long-term non-progressor HIV patients are characterized by altered phenotype and function. Clin Immunol 124(3):277–283PubMedCrossRefGoogle Scholar
  94. 94.
    Arnon TI et al (2005) Inhibition of the NKp30 activating receptor by pp 65 of human cytomegalovirus. Nat Immunol 6(5):515–523PubMedCrossRefGoogle Scholar
  95. 95.
    Golden-Mason L, Rosen HR (2006) Natural killer cells: primary target for hepatitis C virus immune evasion strategies? Liver Transpl 12(3):363–372PubMedCrossRefGoogle Scholar
  96. 96.
    Sinclair J (2008) Human cytomegalovirus: Latency and reactivation in the myeloid lineage. J Clin Virol 41(3):180–185Google Scholar
  97. 97.
    Dunn C et al (2003) Human cytomegalovirus glycoprotein UL16 causes intracellular sequestration of NKG2D ligands, protecting against natural killer cell cytotoxicity. J Exp Med 197(11):1427–1439PubMedCrossRefGoogle Scholar
  98. 98.
    Cosman D et al (2001) ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 14(2):123–133PubMedCrossRefGoogle Scholar
  99. 99.
    Kubin M et al (2001) ULBP1, 2, 3: novel MHC class I-related molecules that bind to human cytomegalovirus glycoprotein UL16, activate NK cells. Eur J Immunol 31(5):1428–1437PubMedCrossRefGoogle Scholar
  100. 100.
    Krmpotic A et al (2005) NK cell activation through the NKG2D ligand MULT-1 is selectively prevented by the glycoprotein encoded by mouse cytomegalovirus gene m145. J Exp Med 201(2):211–220PubMedCrossRefGoogle Scholar
  101. 101.
    Lodoen M et al (2003) NKG2D-mediated natural killer cell protection against cytomegalovirus is impaired by viral gp40 modulation of retinoic acid early inducible 1 gene molecules. J Exp Med 197(10):1245–1253PubMedCrossRefGoogle Scholar
  102. 102.
    Hasan M et al (2005) Selective down-regulation of the NKG2D ligand H60 by mouse cytomegalovirus m155 glycoprotein. J Virol 79(5):2920–2930PubMedCrossRefGoogle Scholar
  103. 103.
    Lodoen MB et al (2004) The cytomegalovirus m155 gene product subverts natural killer cell antiviral protection by disruption of H60-NKG2D interactions. J Exp Med 200(8):1075–1081PubMedCrossRefGoogle Scholar
  104. 104.
    Krmpotic A et al (2002) MCMV glycoprotein gp40 confers virus resistance to CD8+ T cells and NK cells in vivo. Nat Immunol 3(6):529–535PubMedCrossRefGoogle Scholar
  105. 105.
    Lenac T et al (2008) Murine cytomegalovirus regulation of NKG2D ligands. Med Microbiol Immunol 197(2):159–166PubMedCrossRefGoogle Scholar
  106. 106.
    Lenac T et al (2006) The herpesviral Fc receptor fcr-1 down-regulates the NKG2D ligands MULT-1 and H60. J Exp Med 203(8):1843–1850PubMedCrossRefGoogle Scholar
  107. 107.
    Mintern JD et al (2006) Viral interference with B7–1 costimulation: a new role for murine cytomegalovirus fc receptor-1. J Immunol 177(12):8422–8431PubMedGoogle Scholar
  108. 108.
    Arapovic J et al (2009) Promiscuity of MCMV immunoevasin of NKG2D: m138/fcr-1 down-modulates RAE-1ε in addition to MULT-1 and H60. Mol ImmunolGoogle Scholar
  109. 109.
    Cerwenka A, Baron JL, Lanier LL (2001) Ectopic expression of retinoic acid early inducible-1 gene (RAE-1) permits natural killer cell-mediated rejection of a MHC class I-bearing tumor in vivo. Proc Natl Acad Sci USA 98(20):11521–11526PubMedCrossRefGoogle Scholar
  110. 110.
    Regunathan J et al (2005) NKG2D receptor-mediated NK cell function is regulated by inhibitory Ly49 receptors. Blood 105(1):233–240PubMedCrossRefGoogle Scholar
  111. 111.
    Coscoy L (2007) Immune evasion by Kaposi's sarcoma-associated herpesvirus. Nat Rev Immunol 7(5):391–401PubMedCrossRefGoogle Scholar
  112. 112.
    Thomas M et al (2008) Down-regulation of NKG2D and NKp80 ligands by Kaposi's sarcoma-associated herpesvirus K5 protects against NK cell cytotoxicity. Proc Natl Acad Sci USA 105(5):1656–1661PubMedCrossRefGoogle Scholar
  113. 113.
    Chalupny NJ et al (2006) Down-regulation of the NKG2D ligand MICA by the human cytomegalovirus glycoprotein UL142. Biochem Biophys Res Commun 346(1):175–181PubMedCrossRefGoogle Scholar
  114. 114.
    Zou Y et al (2005) Effect of human cytomegalovirus on expression of MHC class I-related chains A. J Immunol 174(5):3098–3104PubMedGoogle Scholar
  115. 115.
    Cerboni C et al (2007) Human immunodeficiency virus 1 Nef protein downmodulates the ligands of the activating receptor NKG2D and inhibits natural killer cell-mediated cytotoxicity. J Gen Virol 88(Pt 1):242–250PubMedCrossRefGoogle Scholar
  116. 116.
    Zheng ZY, Zucker-Franklin D (1992) Apparent ineffectiveness of natural killer cells vis-a-vis retrovirus-infected targets. J Immunol 148(11):3679–3685PubMedGoogle Scholar
  117. 117.
    Owen RE et al (2007) Alterations in receptor binding properties of recent human influenza H3N2 viruses are associated with reduced natural killer cell lysis of infected cells. J Virol 81(20):11170–11178PubMedCrossRefGoogle Scholar
  118. 118.
    Campbell JA et al (2007) Zoonotic orthopoxviruses encode a high-affinity antagonist of NKG2D. J Exp Med 204(6):1311–1317PubMedCrossRefGoogle Scholar
  119. 119.
    Groh V et al (2002) Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 419(6908):734–738PubMedCrossRefGoogle Scholar
  120. 120.
    Groh V et al (2001) Costimulation of CD8alphabeta T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat Immunol 2(3):255–260PubMedCrossRefGoogle Scholar
  121. 121.
    Fletcher JM, Prentice HG, Grundy JE (1998) Natural killer cell lysis of cytomegalovirus (CMV)-infected cells correlates with virally induced changes in cell surface lymphocyte function-associated antigen-3 (LFA-3) expression and not with the CMV-induced down-regulation of cell surface class I HLA. J Immunol 161(5):2365–2374PubMedGoogle Scholar
  122. 122.
    Orange JS et al (2002) Viral evasion of natural killer cells. Nat Immunol 3(11):1006–1012PubMedCrossRefGoogle Scholar
  123. 123.
    Coscoy L, Sanchez DJ, Ganem D (2001) A novel class of herpesvirus-encoded membrane-bound E3 ubiquitin ligases regulates endocytosis of proteins involved in immune recognition. J Cell Biol 155(7):1265–1273PubMedCrossRefGoogle Scholar
  124. 124.
    Coscoy L, Ganem D (2001) A viral protein that selectively downregulates ICAM-1 and B7–2 and modulates T cell costimulation. J Clin Invest 107(12):1599–1606PubMedCrossRefGoogle Scholar
  125. 125.
    Hildreth JE et al (1983) A human lymphocyte-associated antigen involved in cell-mediated lympholysis. Eur J Immunol 13(3):202–208PubMedCrossRefGoogle Scholar
  126. 126.
    Miedema F et al (1984) Both Fc receptors and lymphocyte-function-associated antigen 1 on human T gamma lymphocytes are required for antibody-dependent cellular cytotoxicity (killer cell activity). Eur J Immunol 14(6):518–523PubMedCrossRefGoogle Scholar
  127. 127.
    Banerjee P, Feuer G, Barker E (2007) Human T-cell leukemia virus type 1 (HTLV-1) p12I down-modulates ICAM-1 and -2 and reduces adherence of natural killer cells, thereby protecting HTLV-1-infected primary CD4+ T cells from autologous natural killer cell-mediated cytotoxicity despite the reduction of major histocompatibility complex class I molecules on infected cells. J Virol 81(18):9707–9717PubMedCrossRefGoogle Scholar
  128. 128.
    Crotta S et al (2002) Inhibition of natural killer cells through engagement of CD81 by the major hepatitis C virus envelope protein. J Exp Med 195(1):35–41PubMedCrossRefGoogle Scholar
  129. 129.
    Pedersen I, David M (2008) MicroRNAs in the immune response. Cytokine 43(3):391–394PubMedCrossRefGoogle Scholar
  130. 130.
    Gottwein E, Cullen BR (2008) Viral and cellular microRNAs as determinants of viral pathogenesis and immunity. Cell Host Microbe 3(6):375–387PubMedCrossRefGoogle Scholar
  131. 131.
    Zhang G et al (2007) Antisense transcription in the human cytomegalovirus transcriptome. J Virol 81(20):11267–11281PubMedCrossRefGoogle Scholar
  132. 132.
    Sullivan CS et al (2005) SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells. Nature 435(7042):682–686PubMedCrossRefGoogle Scholar
  133. 133.
    Stern-Ginossar N et al (2007) Host immune system gene targeting by a viral miRNA. Science 317(5836):376–381PubMedCrossRefGoogle Scholar
  134. 134.
    Murphy E et al (2008) Suppression of immediate-early viral gene expression by herpesvirus-coded microRNAs: implications for latency. Proc Natl Acad Sci USA 105(14):5453–5458PubMedCrossRefGoogle Scholar
  135. 135.
    Grey F et al (2007) A human cytomegalovirus-encoded microRNA regulates expression of multiple viral genes involved in replication. PLoS Pathog 3(11):e163CrossRefGoogle Scholar
  136. 136.
    Scalzo AA et al (1992) The effect of the Cmv-1 resistance gene, which is linked to the natural killer cell gene complex, is mediated by natural killer cells. J Immunol 149(2):581–589PubMedGoogle Scholar
  137. 137.
    Voigt V et al (2003) Murine cytomegalovirus m157 mutation and variation leads to immune evasion of natural killer cells. Proc Natl Acad Sci USA 100(23):13483–13488PubMedCrossRefGoogle Scholar
  138. 138.
    French AR et al (2004) Escape of mutant double-stranded DNA virus from innate immune control. Immunity 20(6):747–756PubMedCrossRefGoogle Scholar
  139. 139.
    Makrigiannis AP et al (2001) Class I MHC-binding characteristics of the 129/J Ly49 repertoire. J Immunol 166(8):5034–5043PubMedGoogle Scholar
  140. 140.
    Abi-Rached L, Parham P (2005) Natural selection drives recurrent formation of activating killer cell immunoglobulin-like receptor and Ly49 from inhibitory homologues. J Exp Med 201(8):1319–1332PubMedCrossRefGoogle Scholar
  141. 141.
    Adam SG et al (2006) Cmv4, a new locus linked to the NK cell gene complex, controls innate resistance to cytomegalovirus in wild-derived mice. J Immunol 176(9):5478–5485PubMedGoogle Scholar
  142. 142.
    Carlyle JR et al (2006) Molecular and genetic basis for strain-dependent NK1.1 alloreactivity of mouse NK cells. J Immunol 176(12):7511–7524PubMedGoogle Scholar
  143. 143.
    Alter G et al (2007) Differential natural killer cell-mediated inhibition of HIV-1 replication based on distinct KIR/HLA subtypes. J Exp Med 204(12):3027–3036PubMedCrossRefGoogle Scholar
  144. 144.
    Khakoo SI et al (2004) HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science 305(5685):872–874PubMedCrossRefGoogle Scholar
  145. 145.
    Lanier LL (2008) Evolutionary struggles between NK cells and viruses. Nat Rev Immunol 8(4):259–268PubMedCrossRefGoogle Scholar
  146. 146.
    Kloover JS et al (2002) A rat cytomegalovirus strain with a disruption of the r144 MHC class I-like gene is attenuated in the acute phase of infection in neonatal rats. Arch Virol 147(4):813–824PubMedCrossRefGoogle Scholar
  147. 147.
    Llano M et al (2003) Differential effects of US2, US6 and US11 human cytomegalovirus proteins on HLA class Ia and HLA-E expression: impact on target susceptibility to NK cell subsets. Eur J Immunol 33(10):2744–2754PubMedCrossRefGoogle Scholar
  148. 148.
    Hengel H et al (1997) A viral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter. Immunity 6(5):623–632PubMedCrossRefGoogle Scholar
  149. 149.
    Ahn K et al (1997) The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity 6(5):613–621PubMedCrossRefGoogle Scholar
  150. 150.
    Barel MT et al (2003) Human cytomegalovirus-encoded US2 differentially affects surface expression of MHC class I locus products and targets membrane-bound, but not soluble HLA-G1 for degradation. J Immunol 171(12):6757–6765PubMedGoogle Scholar
  151. 151.
    Schust DJ et al (1998) Trophoblast class I major histocompatibility complex (MHC) products are resistant to rapid degradation imposed by the human cytomegalovirus (HCMV) gene products US2 and US11. J Exp Med 188(3):497–503PubMedCrossRefGoogle Scholar
  152. 152.
    Wiertz EJ et al (1996) The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84(5):769–779PubMedCrossRefGoogle Scholar
  153. 153.
    Wiertz EJ et al (1996) Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384(6608):432–438PubMedCrossRefGoogle Scholar
  154. 154.
    Jones TR et al (1996) Human cytomegalovirus US3 impairs transport and maturation of major histocompatibility complex class I heavy chains. Proc Natl Acad Sci USA 93(21):11327–11333PubMedCrossRefGoogle Scholar
  155. 155.
    Misaghi S et al (2004) Structural and functional analysis of human cytomegalovirus US3 protein. J Virol 78(1):413–423PubMedCrossRefGoogle Scholar
  156. 156.
    Furman MH et al (2002) The human cytomegalovirus US10 gene product delays trafficking of major histocompatibility complex class I molecules. J Virol 76(22):11753–11756PubMedCrossRefGoogle Scholar
  157. 157.
    Greenberg ME, Iafrate AJ, Skowronski J (1998) The SH3 domain-binding surface and an acidic motif in HIV-1 Nef regulate trafficking of class I MHC complexes. EMBO J 17(10):2777–2789PubMedCrossRefGoogle Scholar
  158. 158.
    Le Gall S et al (1998) Nef interacts with the mu subunit of clathrin adaptor complexes and reveals a cryptic sorting signal in MHC I molecules. Immunity 8(4):483–495PubMedCrossRefGoogle Scholar
  159. 159.
    Tomasec P et al (2005) Downregulation of natural killer cell-activating ligand CD155 by human cytomegalovirus UL141. Nat Immunol 6(2):181–188PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  • Vanda Juranić Lisnić
    • 1
  • Iva Gašparović
    • 1
  • Astrid Krmpotić
    • 1
  • Stipan Jonjić
    • 1
    Email author
  1. 1.Department of Histology and EmbryologyFaculty of MedicineRijekaCroatia

Personalised recommendations