1932

Abstract

The continuous interactions between host and pathogens during their coevolution have shaped both the immune system and the countermeasures used by pathogens. Natural killer (NK) cells are innate lymphocytes that are considered central players in the antiviral response. Not only do they express a variety of inhibitory and activating receptors to discriminate and eliminate target cells but they can also produce immunoregulatory cytokines to alert the immune system. Reciprocally, several unrelated viruses including cytomegalovirus, human immunodeficiency virus, influenza virus, and dengue virus have evolved a multitude of mechanisms to evade NK cell function, such as the targeting of pathways for NK cell receptors and their ligands, apoptosis, and cytokine-mediated signaling. The studies discussed in this article provide further insights into the antiviral function of NK cells and the pathways involved, their constituent proteins, and ways in which they could be manipulated for host benefit.

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2020-04-26
2024-12-10
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Literature Cited

  1. 1. 
    Enard D, Cai L, Gwennap C, Petrov DA 2016. Viruses are a dominant driver of protein adaptation in mammals. eLife 5:e12469
    [Google Scholar]
  2. 2. 
    Biron CA, Byron KS, Sullivan JL 1989. Severe herpesvirus infections in an adolescent without natural killer cells. N. Engl. J. Med. 320:1731–35
    [Google Scholar]
  3. 3. 
    Spits H, Artis D, Colonna M, Diefenbach A, Di Santo JP et al. 2013. Innate lymphoid cells—a proposal for uniform nomenclature. Nat. Rev. Immunol. 13:145–49
    [Google Scholar]
  4. 4. 
    Spits H, Bernink JH, Lanier L 2016. NK cells and type 1 innate lymphoid cells: partners in host defense. Nat. Immunol. 17:758–64
    [Google Scholar]
  5. 5. 
    Trinchieri G. 1989. Biology of natural killer cells. Adv. Immunol. 47:187–376
    [Google Scholar]
  6. 6. 
    Mace EM, Orange JS. 2019. Emerging insights into human health and NK cell biology from the study of NK cell deficiencies. Immunol. Rev. 287:202–25
    [Google Scholar]
  7. 7. 
    Belkaya S, Michailidis E, Korol CB, Kabbani M, Cobat A et al. 2019. Inherited IL-18BP deficiency in human fulminant viral hepatitis. J. Exp. Med. 216:1777–90
    [Google Scholar]
  8. 8. 
    Zhang J, Marotel M, Fauteux-Daniel S, Mathieu AL, Viel S et al. 2018. T-bet and Eomes govern differentiation and function of mouse and human NK cells and ILC1. Eur. J. Immunol. 48:738–50
    [Google Scholar]
  9. 9. 
    Seillet C, Belz GT, Huntington ND 2016. Development, homeostasis, and heterogeneity of NK cells and ILC1. Curr. Top. Microbiol. Immunol. 395:37–61
    [Google Scholar]
  10. 10. 
    Gaynor LM, Colucci F. 2017. Uterine natural killer cells: functional distinctions and influence on pregnancy in humans and mice. Front. Immunol. 8:467
    [Google Scholar]
  11. 11. 
    Morvan MG, Lanier LL. 2016. NK cells and cancer: you can teach innate cells new tricks. Nat. Rev. Cancer 16:7–19
    [Google Scholar]
  12. 12. 
    Chiossone L, Dumas PY, Vienne M, Vivier E 2018. Natural killer cells and other innate lymphoid cells in cancer. Nat. Rev. Immunol. 18:671–88
    [Google Scholar]
  13. 13. 
    Marcais A, Viel S, Grau M, Henry T, Marvel J, Walzer T 2013. Regulation of mouse NK cell development and function by cytokines. Front. Immunol. 4:450
    [Google Scholar]
  14. 14. 
    Vidal SM, Khakoo SI, Biron CA 2011. Natural killer cell responses during viral infections: flexibility and conditioning of innate immunity by experience. Curr. Opin. Virol. 1:497–512
    [Google Scholar]
  15. 15. 
    Gregoire C, Chasson L, Luci C, Tomasello E, Geissmann F et al. 2007. The trafficking of natural killer cells. Immunol. Rev. 220:169–82
    [Google Scholar]
  16. 16. 
    Prager I, Watzl C. 2019. Mechanisms of natural killer cell-mediated cellular cytotoxicity. J. Leukoc. Biol. 105:1319–29
    [Google Scholar]
  17. 17. 
    Yokoyama WM, Seaman WE. 1993. The Ly-49 and NKR-P1 gene families encoding lectin-like receptors on natural killer cells: the NK gene complex. Annu. Rev. Immunol. 11:613–35
    [Google Scholar]
  18. 18. 
    Bryceson YT, March ME, Ljunggren HG, Long EO 2006. Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood 107:159–66
    [Google Scholar]
  19. 19. 
    Bastidas-Legarda LY, Khakoo SI. 2019. Conserved and variable natural killer cell receptors: diverse approaches to viral infections. Immunology 156:319–28
    [Google Scholar]
  20. 20. 
    Barrow AD, Martin CJ, Colonna M 2019. The natural cytotoxicity receptors in health and disease. Front. Immunol. 10:909
    [Google Scholar]
  21. 21. 
    Martinet L, Smyth MJ. 2015. Balancing natural killer cell activation through paired receptors. Nat. Rev. Immunol. 15:243–54
    [Google Scholar]
  22. 22. 
    Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L et al. 2011. Innate or adaptive immunity? The example of natural killer cells. Science 331:44–49
    [Google Scholar]
  23. 23. 
    Kim S, Poursine-Laurent J, Truscott SM, Lybarger L, Song YJ et al. 2005. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 436:709–13
    [Google Scholar]
  24. 24. 
    Brodin P, Lakshmikanth T, Johansson S, Karre K, Hoglund P 2009. The strength of inhibitory input during education quantitatively tunes the functional responsiveness of individual natural killer cells. Blood 113:2434–41
    [Google Scholar]
  25. 25. 
    Held W, Roland J, Raulet DH 1995. Allelic exclusion of Ly49-family genes encoding class I MHC-specific receptors on NK cells. Nature 376:355–58
    [Google Scholar]
  26. 26. 
    Dokun AO, Kim S, Smith HR, Kang HS, Chu DT, Yokoyama WM 2001. Specific and nonspecific NK cell activation during virus infection. Nat. Immunol. 2:951–56
    [Google Scholar]
  27. 27. 
    Lee SH, Kim KS, Fodil-Cornu N, Vidal SM, Biron CA 2009. Activating receptors promote NK cell expansion for maintenance, IL-10 production, and CD8 T cell regulation during viral infection. J. Exp. Med. 206:2235–51
    [Google Scholar]
  28. 28. 
    Sun JC, Beilke JN, Lanier LL 2009. Adaptive immune features of natural killer cells. Nature 457:557–61
    [Google Scholar]
  29. 29. 
    Paust S, Blish CA, Reeves RK 2017. Redefining memory: building the case for adaptive NK cells. J. Virol. 91:e00169–17
    [Google Scholar]
  30. 30. 
    Luetke-Eversloh M, Hammer Q, Durek P, Nordstrom K, Gasparoni G et al. 2014. Human cytomegalovirus drives epigenetic imprinting of the IFNG locus in NKG2Chi natural killer cells. PLOS Pathog 10:e1004441
    [Google Scholar]
  31. 31. 
    Lau CM, Adams NM, Geary CD, Weizman OE, Rapp M et al. 2018. Epigenetic control of innate and adaptive immune memory. Nat. Immunol. 19:963–72
    [Google Scholar]
  32. 32. 
    Crinier A, Milpied P, Escaliere B, Piperoglou C, Galluso J et al. 2018. High-dimensional single-cell analysis identifies organ-specific signatures and conserved NK cell subsets in humans and mice. Immunity 49:971–86.e5
    [Google Scholar]
  33. 33. 
    Wilk AJ, Blish CA. 2018. Diversification of human NK cells: lessons from deep profiling. J. Leukoc. Biol. 103:629–41
    [Google Scholar]
  34. 34. 
    Carrillo-Bustamante P, Kesmir C, de Boer RJ 2016. The evolution of natural killer cell receptors. Immunogenetics 68:3–18
    [Google Scholar]
  35. 35. 
    van Erp EA, van Kampen MR, van Kasteren PB, de Wit J 2019. Viral infection of human natural killer cells. Viruses 11:E243
    [Google Scholar]
  36. 36. 
    Campbell TM, McSharry BP, Steain M, Russell TA, Tscharke DC et al. 2019. Functional paralysis of human natural killer cells by alphaherpesviruses. PLOS Pathog 15:e1007784
    [Google Scholar]
  37. 37. 
    Campbell TM, McSharry BP, Steain M, Ashhurst TM, Slobedman B, Abendroth A 2018. Varicella zoster virus productively infects human natural killer cells and manipulates phenotype. PLOS Pathog 14:e1006999
    [Google Scholar]
  38. 38. 
    Tabiasco J, Vercellone A, Meggetto F, Hudrisier D, Brousset P, Fournie JJ 2003. Acquisition of viral receptor by NK cells through immunological synapse. J. Immunol. 170:5993–98
    [Google Scholar]
  39. 39. 
    Isobe Y, Sugimoto K, Yang L, Tamayose K, Egashira M et al. 2004. Epstein-Barr virus infection of human natural killer cell lines and peripheral blood natural killer cells. Cancer Res 64:2167–74
    [Google Scholar]
  40. 40. 
    Williams LR, Quinn LL, Rowe M, Zuo J 2016. Induction of the lytic cycle sensitizes Epstein-Barr virus-infected B cells to NK cell killing that is counteracted by virus-mediated NK cell evasion mechanisms in the late lytic cycle. J. Virol. 90:947–58
    [Google Scholar]
  41. 41. 
    Sarid R, Sato T, Bohenzky RA, Russo JJ, Chang Y 1997. Kaposi's sarcoma-associated herpesvirus encodes a functional bcl-2 homologue. Nat. Med. 3:293–98
    [Google Scholar]
  42. 42. 
    Juhasova B, Bhatia-Kissova I, Polcicova K, Mentel M, Forte M, Polcic P 2011. Reconstitution of interactions of Murine gammaherpesvirus 68 M11 with Bcl-2 family proteins in yeast. Biochem. Biophys. Res. Commun. 407:783–87
    [Google Scholar]
  43. 43. 
    Harada H, Goto Y, Ohno T, Suzu S, Okada S 2007. Proliferative activation up-regulates expression of CD4 and HIV-1 co-receptors on NK cells and induces their infection with HIV-1. Eur. J. Immunol. 37:2148–55
    [Google Scholar]
  44. 44. 
    Valentin A, Rosati M, Patenaude DJ, Hatzakis A, Kostrikis LG et al. 2002. Persistent HIV-1 infection of natural killer cells in patients receiving highly active antiretroviral therapy. PNAS 99:7015–20
    [Google Scholar]
  45. 45. 
    Bernstein HB, Wang G, Plasterer MC, Zack JA, Ramasastry P et al. 2009. CD4+ NK cells can be productively infected with HIV, leading to downregulation of CD4 expression and changes in function. Virology 387:59–66
    [Google Scholar]
  46. 46. 
    Alvarez-Breckenridge CA, Yu J, Price R, Wojton J, Pradarelli J et al. 2012. NK cells impede glioblastoma virotherapy through NKp30 and NKp46 natural cytotoxicity receptors. Nat. Med. 18:1827–34
    [Google Scholar]
  47. 47. 
    Mandelboim O, Lieberman N, Lev M, Paul L, Arnon TI et al. 2001. Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 409:1055–60
    [Google Scholar]
  48. 48. 
    Arnon TI, Lev M, Katz G, Chernobrov Y, Porgador A, Mandelboim O 2001. Recognition of viral hemagglutinins by NKp44 but not by NKp30. Eur. J. Immunol. 31:2680–89
    [Google Scholar]
  49. 49. 
    Mao H, Tu W, Qin G, Law HK, Sia SF et al. 2009. Influenza virus directly infects human natural killer cells and induces cell apoptosis. J. Virol. 83:9215–22
    [Google Scholar]
  50. 50. 
    Mao H, Tu W, Liu Y, Qin G, Zheng J et al. 2010. Inhibition of human natural killer cell activity by influenza virions and hemagglutinin. J. Virol. 84:4148–57
    [Google Scholar]
  51. 51. 
    Du N, Zhou J, Lin X, Zhang Y, Yang X et al. 2010. Differential activation of NK cells by influenza A pseudotype H5N1 and 1918 and 2009 pandemic H1N1 viruses. J. Virol. 84:7822–31
    [Google Scholar]
  52. 52. 
    Lin SJ, Cheng PJ, Lin TY, Lee PT, Hsiao HS, Kuo ML 2012. Effect of influenza A infection on umbilical cord blood natural killer function regulation with interleukin-15. J. Infect. Dis. 205:745–56
    [Google Scholar]
  53. 53. 
    Mao H, Liu Y, Sia SF, Peiris JSM, Lau YL, Tu W 2017. Avian influenza virus directly infects human natural killer cells and inhibits cell activity. Virol. Sin. 32:122–29
    [Google Scholar]
  54. 54. 
    Chisholm SE, Reyburn HT. 2006. Recognition of vaccinia virus-infected cells by human natural killer cells depends on natural cytotoxicity receptors. J. Virol. 80:2225–33
    [Google Scholar]
  55. 55. 
    Jarahian M, Fiedler M, Cohnen A, Djandji D, Hammerling GJ et al. 2011. Modulation of NKp30- and NKp46-mediated natural killer cell responses by poxviral hemagglutinin. PLOS Pathog 7:e1002195
    [Google Scholar]
  56. 56. 
    Hershkovitz O, Rosental B, Rosenberg LA, Navarro-Sanchez ME, Jivov S et al. 2009. NKp44 receptor mediates interaction of the envelope glycoproteins from the West Nile and dengue viruses with NK cells. J. Immunol. 183:2610–21
    [Google Scholar]
  57. 57. 
    Arnon TI, Achdout H, Levi O, Markel G, Saleh N et al. 2005. Inhibition of the NKp30 activating receptor by pp65 of human cytomegalovirus. Nat. Immunol. 6:515–23
    [Google Scholar]
  58. 58. 
    Yoon JC, Shiina M, Ahlenstiel G, Rehermann B 2009. Natural killer cell function is intact after direct exposure to infectious hepatitis C virions. Hepatology 49:12–21
    [Google Scholar]
  59. 59. 
    Holder KA, Stapleton SN, Gallant ME, Russell RS, Grant MD 2013. Hepatitis C virus-infected cells downregulate NKp30 and inhibit ex vivo NK cell functions. J. Immunol. 191:3308–18
    [Google Scholar]
  60. 60. 
    Song H, Josleyn N, Janosko K, Skinner J, Reeves RK et al. 2013. Monkeypox virus infection of rhesus macaques induces massive expansion of natural killer cells but suppresses natural killer cell functions. PLOS ONE 8:e77804
    [Google Scholar]
  61. 61. 
    Parker AK, Parker S, Yokoyama WM, Corbett JA, Buller RM 2007. Induction of natural killer cell responses by ectromelia virus controls infection. J. Virol. 81:4070–79
    [Google Scholar]
  62. 62. 
    Gandini M, Petitinga-Paiva F, Marinho CF, Correa G, De Oliveira-Pinto LM et al. 2017. Dengue virus induces NK cell activation through TRAIL expression during infection. Mediators Inflamm 2017:5649214
    [Google Scholar]
  63. 63. 
    Nachtwey J, Spencer JV. 2008. HCMV IL-10 suppresses cytokine expression in monocytes through inhibition of nuclear factor-κB. Viral Immunol. 21:477–82
    [Google Scholar]
  64. 64. 
    Jochum S, Moosmann A, Lang S, Hammerschmidt W, Zeidler R 2012. The EBV immunoevasins vIL-10 and BNLF2a protect newly infected B cells from immune recognition and elimination. PLOS Pathog 8:e1002704
    [Google Scholar]
  65. 65. 
    Born TL, Morrison LA, Esteban DJ, VandenBos T, Thebeau LG et al. 2000. A poxvirus protein that binds to and inactivates IL-18, and inhibits NK cell response. J. Immunol. 164:3246–54
    [Google Scholar]
  66. 66. 
    Reading PC, Smith GL. 2003. Vaccinia virus interleukin-18-binding protein promotes virulence by reducing gamma interferon production and natural killer and T-cell activity. J. Virol. 77:9960–68
    [Google Scholar]
  67. 67. 
    Xiang Y, Moss B. 1999. IL-18 binding and inhibition of interferon gamma induction by human poxvirus-encoded proteins. PNAS 96:11537–42
    [Google Scholar]
  68. 68. 
    Lee SJ, Cho YS, Cho MC, Shim JH, Lee KA et al. 2001. Both E6 and E7 oncoproteins of human papillomavirus 16 inhibit IL-18-induced IFN-gamma production in human peripheral blood mononuclear and NK cells. J. Immunol. 167:497–504
    [Google Scholar]
  69. 69. 
    Penfold ME, Dairaghi DJ, Duke GM, Saederup N, Mocarski ES et al. 1999. Cytomegalovirus encodes a potent alpha chemokine. PNAS 96:9839–44
    [Google Scholar]
  70. 70. 
    Waldhoer M, Kledal TN, Farrell H, Schwartz TW 2002. Murine cytomegalovirus (CMV) M33 and human CMV US28 receptors exhibit similar constitutive signaling activities. J. Virol. 76:8161–68
    [Google Scholar]
  71. 71. 
    Milne RS, Mattick C, Nicholson L, Devaraj P, Alcami A, Gompels UA 2000. RANTES binding and down-regulation by a novel human herpesvirus-6 β chemokine receptor. J. Immunol. 164:2396–404
    [Google Scholar]
  72. 72. 
    Catusse J, Spinks J, Mattick C, Dyer A, Laing K et al. 2008. Immunomodulation by herpesvirus U51A chemokine receptor via CCL5 and FOG-2 down-regulation plus XCR1 and CCR7 mimicry in human leukocytes. Eur. J. Immunol. 38:763–77
    [Google Scholar]
  73. 73. 
    Isegawa Y, Ping Z, Nakano K, Sugimoto N, Yamanishi K 1998. Human herpesvirus 6 open reading frame U12 encodes a functional beta-chemokine receptor. J. Virol. 72:6104–12
    [Google Scholar]
  74. 74. 
    Nakano K, Tadagaki K, Isegawa Y, Aye MM, Zou P, Yamanishi K 2003. Human herpesvirus 7 open reading frame U12 encodes a functional β-chemokine receptor. J. Virol. 77:8108–15
    [Google Scholar]
  75. 75. 
    Tadagaki K, Nakano K, Yamanishi K 2005. Human herpesvirus 7 open reading frames U12 and U51 encode functional β-chemokine receptors. J. Virol. 79:7068–76
    [Google Scholar]
  76. 76. 
    Yamin R, Kaynan NS, Glasner A, Vitenshtein A, Tsukerman P et al. 2013. The viral KSHV chemokine vMIP-II inhibits the migration of naive and activated human NK cells by antagonizing two distinct chemokine receptors. PLOS Pathog 9:e1003568
    [Google Scholar]
  77. 77. 
    Zocchi MR, Rubartelli A, Morgavi P, Poggi A 1998. HIV-1 Tat inhibits human natural killer cell function by blocking L-type calcium channels. J. Immunol. 161:2938–43
    [Google Scholar]
  78. 78. 
    Yang CM, Yoon JC, Park JH, Lee JM 2017. Hepatitis C virus impairs natural killer cell activity via viral serine protease NS3. PLOS ONE 12:e0175793
    [Google Scholar]
  79. 79. 
    Johnson DC, Frame MC, Ligas MW, Cross AM, Stow ND 1988. Herpes simplex virus immunoglobulin G Fc receptor activity depends on a complex of two viral glycoproteins, gE and gI. J. Virol. 62:1347–54
    [Google Scholar]
  80. 80. 
    Litwin V, Jackson W, Grose C 1992. Receptor properties of two varicella-zoster virus glycoproteins, gpI and gpIV, homologous to herpes simplex virus gE and gI. J. Virol. 66:3643–51
    [Google Scholar]
  81. 81. 
    Atalay R, Zimmermann A, Wagner M, Borst E, Benz C et al. 2002. Identification and expression of human cytomegalovirus transcription units coding for two distinct Fcγ receptor homologs. J. Virol. 76:8596–608
    [Google Scholar]
  82. 82. 
    Corrales-Aguilar E, Trilling M, Hunold K, Fiedler M, Le VT et al. 2014. Human cytomegalovirus Fcγ binding proteins gp34 and gp68 antagonize Fcγ receptors I, II and III. PLOS Pathog 10:e1004131
    [Google Scholar]
  83. 83. 
    Kolb P, Sijmons S, McArdle MR, Taher H, Womack J et al. 2019. Identification and functional characterization of a novel Fc gamma-binding glycoprotein in rhesus cytomegalovirus. J. Virol. 93:e02077–18
    [Google Scholar]
  84. 84. 
    Stanton RJ, Prod'homme V, Purbhoo MA, Moore M, Aicheler RJ et al. 2014. HCMV pUL135 remodels the actin cytoskeleton to impair immune recognition of infected cells. Cell Host Microbe 16:201–14
    [Google Scholar]
  85. 85. 
    Wang ECY, Pjechova M, Nightingale K, Vlahava VM, Patel M et al. 2018. Suppression of costimulation by human cytomegalovirus promotes evasion of cellular immune defenses. PNAS 115:4998–5003
    [Google Scholar]
  86. 86. 
    Smith W, Tomasec P, Aicheler R, Loewendorf A, Nemcovicova I et al. 2013. Human cytomegalovirus glycoprotein UL141 targets the TRAIL death receptors to thwart host innate antiviral defenses. Cell Host Microbe 13:324–35
    [Google Scholar]
  87. 87. 
    Verma S, Loewendorf A, Wang Q, McDonald B, Redwood A, Benedict CA 2014. Inhibition of the TRAIL death receptor by CMV reveals its importance in NK cell-mediated antiviral defense. PLOS Pathog 10:e1004268
    [Google Scholar]
  88. 88. 
    Picarda G, Ghosh R, McDonald B, Verma S, Thiault N et al. 2019. Cytomegalovirus evades TRAIL-mediated innate lymphoid cell 1 defenses. J. Virol. 93:e00617–19
    [Google Scholar]
  89. 89. 
    Wu N, Veillette A. 2016. SLAM family receptors in normal immunity and immune pathologies. Curr. Opin. Immunol. 38:45–51
    [Google Scholar]
  90. 90. 
    Urlaub D, Hofer K, Muller ML, Watzl C 2017. LFA-1 activation in NK cells and their subsets: influence of receptors, maturation, and cytokine stimulation. J. Immunol. 198:1944–51
    [Google Scholar]
  91. 91. 
    Martinez-Vicente P, Farre D, Sanchez C, Alcami A, Engel P, Angulo A 2019. Subversion of natural killer cell responses by a cytomegalovirus-encoded soluble CD48 decoy receptor. PLOS Pathog 15:e1007658
    [Google Scholar]
  92. 92. 
    Zarama A, Perez-Carmona N, Farre D, Tomic A, Borst EM et al. 2014. Cytomegalovirus m154 hinders CD48 cell-surface expression and promotes viral escape from host natural killer cell control. PLOS Pathog 10:e1004000
    [Google Scholar]
  93. 93. 
    Shah AH, Sowrirajan B, Davis ZB, Ward JP, Campbell EM et al. 2010. Degranulation of natural killer cells following interaction with HIV-1-infected cells is hindered by downmodulation of NTB-A by Vpu. Cell Host Microbe 8:397–409
    [Google Scholar]
  94. 94. 
    Martinet L, Ferrari De Andrade L, Guillerey C, Lee JS, Liu J et al. 2015. DNAM-1 expression marks an alternative program of NK cell maturation. Cell Rep 11:85–97
    [Google Scholar]
  95. 95. 
    Bottino C, Castriconi R, Pende D, Rivera P, Nanni M et al. 2003. Identification of PVR (CD155) and Nectin-2 (CD112) as cell surface ligands for the human DNAM-1 (CD226) activating molecule. J. Exp. Med. 198:557–67
    [Google Scholar]
  96. 96. 
    Tomasec P, Wang EC, Davison AJ, Vojtesek B, Armstrong M et al. 2005. Downregulation of natural killer cell-activating ligand CD155 by human cytomegalovirus UL141. Nat. Immunol. 6:181–88
    [Google Scholar]
  97. 97. 
    Prod'homme V, Sugrue DM, Stanton RJ, Nomoto A, Davies J et al. 2010. Human cytomegalovirus UL141 promotes efficient downregulation of the natural killer cell activating ligand CD112. J. Gen. Virol. 91:2034–39
    [Google Scholar]
  98. 98. 
    Lenac Rovis T, Kucan Brlic P, Kaynan N, Juranic Lisnic V, Brizic I et al. 2016. Inflammatory monocytes and NK cells play a crucial role in DNAM-1-dependent control of cytomegalovirus infection. J. Exp. Med. 213:1835–50
    [Google Scholar]
  99. 99. 
    Grauwet K, Cantoni C, Parodi M, De Maria A, Devriendt B et al. 2014. Modulation of CD112 by the alphaherpesvirus gD protein suppresses DNAM-1–dependent NK cell-mediated lysis of infected cells. PNAS 111:16118–23
    [Google Scholar]
  100. 100. 
    Matusali G, Potesta M, Santoni A, Cerboni C, Doria M 2012. The human immunodeficiency virus type 1 Nef and Vpu proteins downregulate the natural killer cell-activating ligand PVR. J. Virol. 86:4496–504
    [Google Scholar]
  101. 101. 
    Galaski J, Ahmad F, Tibroni N, Pujol FM, Muller B et al. 2016. Cell surface downregulation of NK cell ligands by patient-derived HIV-1 Vpu and Nef alleles. J. Acquir. Immune Defic. Syndr. 72:1–10
    [Google Scholar]
  102. 102. 
    Davis ZB, Sowrirajan B, Cogswell A, Ward JP, Planelles V, Barker E 2017. CD155 on HIV-infected cells is not modulated by HIV-1 Vpu and Nef but synergizes with NKG2D ligands to trigger NK cell lysis of autologous primary HIV-infected cells. AIDS Res. Hum. Retroviruses 33:93–100
    [Google Scholar]
  103. 103. 
    Fuchs A, Cella M, Giurisato E, Shaw AS, Colonna M 2004. Cutting edge: CD96 (tactile) promotes NK cell-target cell adhesion by interacting with the poliovirus receptor (CD155). J. Immunol. 172:3994–98
    [Google Scholar]
  104. 104. 
    Stanietsky N, Simic H, Arapovic J, Toporik A, Levy O et al. 2009. The interaction of TIGIT with PVR and PVRL2 inhibits human NK cell cytotoxicity. PNAS 106:17858–63
    [Google Scholar]
  105. 105. 
    Chan CJ, Martinet L, Gilfillan S, Souza-Fonseca-Guimaraes F, Chow MT et al. 2014. The receptors CD96 and CD226 oppose each other in the regulation of natural killer cell functions. Nat. Immunol. 15:431–38
    [Google Scholar]
  106. 106. 
    Kondo M, Maruoka T, Otsuka N, Kasamatsu J, Fugo K et al. 2010. Comparative genomic analysis of mammalian NKG2D ligand family genes provides insights into their origin and evolution. Immunogenetics 62:441–50
    [Google Scholar]
  107. 107. 
    Champsaur M, Lanier LL. 2010. Effect of NKG2D ligand expression on host immune responses. Immunol. Rev. 235:267–85
    [Google Scholar]
  108. 108. 
    Dunn W, Chou C, Li H, Hai R, Patterson D et al. 2003. Functional profiling of a human cytomegalovirus genome. PNAS 100:14223–28
    [Google Scholar]
  109. 109. 
    Welte SA, Sinzger C, Lutz SZ, Singh-Jasuja H, Sampaio KL et al. 2003. Selective intracellular retention of virally induced NKG2D ligands by the human cytomegalovirus UL16 glycoprotein. Eur. J. Immunol. 33:194–203
    [Google Scholar]
  110. 110. 
    Eagle RA, Traherne JA, Hair JR, Jafferji I, Trowsdale J 2009. ULBP6/RAET1L is an additional human NKG2D ligand. Eur. J. Immunol. 39:3207–16
    [Google Scholar]
  111. 111. 
    Muller S, Zocher G, Steinle A, Stehle T 2010. Structure of the HCMV UL16-MICB complex elucidates select binding of a viral immunoevasin to diverse NKG2D ligands. PLOS Pathog 6:e1000723
    [Google Scholar]
  112. 112. 
    Bennett NJ, Ashiru O, Morgan FJ, Pang Y, Okecha G et al. 2010. Intracellular sequestration of the NKG2D ligand ULBP3 by human cytomegalovirus. J. Immunol. 185:1093–102
    [Google Scholar]
  113. 113. 
    Ashiru O, Bennett NJ, Boyle LH, Thomas M, Trowsdale J, Wills MR 2009. NKG2D ligand MICA is retained in the cis-Golgi apparatus by human cytomegalovirus protein UL142. J. Virol. 83:12345–54
    [Google Scholar]
  114. 114. 
    Fielding CA, Aicheler R, Stanton RJ, Wang EC, Han S et al. 2014. Two novel human cytomegalovirus NK cell evasion functions target MICA for lysosomal degradation. PLOS Pathog 10:e1004058
    [Google Scholar]
  115. 115. 
    Schneider CL, Hudson AW. 2011. The human herpesvirus-7 (HHV-7) U21 immunoevasin subverts NK-mediated cytoxicity through modulation of MICA and MICB. PLOS Pathog 7:e1002362
    [Google Scholar]
  116. 116. 
    Sturgill ER, Malouli D, Hansen SG, Burwitz BJ, Seo S et al. 2016. Natural killer cell evasion is essential for infection by rhesus cytomegalovirus. PLOS Pathog 12:e1005868
    [Google Scholar]
  117. 117. 
    Lodoen M, Ogasawara K, Hamerman JA, Arase H, Houchins JP 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. 197:1245–53
    [Google Scholar]
  118. 118. 
    Krmpotic A, Hasan M, Loewendorf A, Saulig T, Halenius 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 201:211–20
    [Google Scholar]
  119. 119. 
    Lenac T, Budt M, Arapovic J, Hasan M, Zimmermann A et al. 2006. The herpesviral Fc receptor fcr-1 down-regulates the NKG2D ligands MULT-1 and H60. J. Exp. Med. 203:1843–50
    [Google Scholar]
  120. 120. 
    Hasan M, Krmpotic A, Ruzsics Z, Bubic I, Lenac T et al. 2005. Selective down-regulation of the NKG2D ligand H60 by mouse cytomegalovirus m155 glycoprotein. J. Virol. 79:2920–30
    [Google Scholar]
  121. 121. 
    Schepis D, D'Amato M, Studahl M, Bergstrom T, Karre K, Berg L 2009. Herpes simplex virus infection downmodulates NKG2D ligand expression. Scand. J. Immunol. 69:429–36
    [Google Scholar]
  122. 122. 
    Campbell TM, McSharry BP, Steain M, Slobedman B, Abendroth A 2015. Varicella-zoster virus and herpes simplex virus 1 differentially modulate NKG2D ligand expression during productive infection. J. Virol. 89:7932–43
    [Google Scholar]
  123. 123. 
    Thomas M, Boname JM, Field S, Nejentsev S, Salio M et al. 2008. Down-regulation of NKG2D and NKp80 ligands by Kaposi's sarcoma-associated herpesvirus K5 protects against NK cell cytotoxicity. PNAS 105:1656–61
    [Google Scholar]
  124. 124. 
    Matthews NC, Goodier MR, Robey RC, Bower M, Gotch FM 2011. Killing of Kaposi's sarcoma-associated herpesvirus-infected fibroblasts during latent infection by activated natural killer cells. Eur. J. Immunol. 41:1958–68
    [Google Scholar]
  125. 125. 
    Stern-Ginossar N, Elefant N, Zimmermann A, Wolf DG, Saleh N et al. 2007. Host immune system gene targeting by a viral miRNA. Science 317:376–81
    [Google Scholar]
  126. 126. 
    Nachmani D, Stern-Ginossar N, Sarid R, Mandelboim O 2009. Diverse herpesvirus microRNAs target the stress-induced immune ligand MICB to escape recognition by natural killer cells. Cell Host Microbe 5:376–85
    [Google Scholar]
  127. 127. 
    Campbell JA, Trossman DS, Yokoyama WM, Carayannopoulos LN 2007. Zoonotic orthopoxviruses encode a high-affinity antagonist of NKG2D. J. Exp. Med. 204:1311–17
    [Google Scholar]
  128. 128. 
    Lazear E, Peterson LW, Nelson CA, Fremont DH 2013. Crystal structure of the cowpox virus-encoded NKG2D ligand OMCP. J. Virol. 87:840–50
    [Google Scholar]
  129. 129. 
    Cerboni C, Neri F, Casartelli N, Zingoni A, Cosman D 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. 88:242–50
    [Google Scholar]
  130. 130. 
    McSharry BP, Burgert HG, Owen DP, Stanton RJ, Prod'homme V et al. 2008. Adenovirus E3/19K promotes evasion of NK cell recognition by intracellular sequestration of the NKG2D ligands major histocompatibility complex class I chain-related proteins A and B. J. Virol. 82:4585–94
    [Google Scholar]
  131. 131. 
    Le Clerc S, Delaneau O, Coulonges C, Spadoni JL, Labib T et al. 2014. Evidence after imputation for a role of MICA variants in nonprogression and elite control of HIV type 1 infection. J. Infect. Dis. 210:1946–50
    [Google Scholar]
  132. 132. 
    Kumar V, Kato N, Urabe Y, Takahashi A, Muroyama R et al. 2011. Genome-wide association study identifies a susceptibility locus for HCV-induced hepatocellular carcinoma. Nat. Genet. 43:455–58
    [Google Scholar]
  133. 133. 
    Garcia G, del Puerto F, Perez AB, Sierra B, Aguirre E et al. 2011. Association of MICA and MICB alleles with symptomatic dengue infection. Hum. Immunol. 72:904–7
    [Google Scholar]
  134. 134. 
    Seidel E, Le VTK, Bar-On Y, Tsukerman P, Enk J et al. 2015. Dynamic co-evolution of host and pathogen: HCMV downregulates the prevalent allele MICA *008 to escape elimination by NK cells. Cell Rep 10:968–82
    [Google Scholar]
  135. 135. 
    Karre K, Ljunggren HG, Piontek G, Kiessling R 1986. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 319:675–78
    [Google Scholar]
  136. 136. 
    Pyzik M, Gendron-Pontbriand EM, Fodil-Cornu N, Vidal SM 2011. Self or nonself? That is the question: sensing of cytomegalovirus infection by innate immune receptors. Mamm. Genome 22:6–18
    [Google Scholar]
  137. 137. 
    Balaji GR, Aguilar OA, Tanaka M, Shingu-Vazquez MA, Fu Z et al. 2018. Recognition of host Clr-b by the inhibitory NKR-P1B receptor provides a basis for missing-self recognition. Nat. Commun. 9:4623
    [Google Scholar]
  138. 138. 
    Braud VM, Allan DS, O'Callaghan CA, Soderstrom K, D'Andrea A et al. 1998. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391:795–99
    [Google Scholar]
  139. 139. 
    Pyzik M, Dumaine A, Charbonneau B, Fodil-Cornu N, Jonjic S, Vidal SM 2014. Viral MHC class I-like molecule allows evasion of NK cell effector responses in vivo. J. Immunol. 193:6061–69
    [Google Scholar]
  140. 140. 
    Železnjak J, Lisnić VJ, Popović B, Lisnić B, Babić M et al. 2019. The complex of MCMV proteins and MHC class I evades NK cell control and drives the evolution of virus-specific activating Ly49 receptors. J. Exp. Med. 216:1809–27
    [Google Scholar]
  141. 141. 
    Holtappels R, Gillert-Marien D, Thomas D, Podlech J, Deegen P et al. 2006. Cytomegalovirus encodes a positive regulator of antigen presentation. J. Virol. 80:7613–24
    [Google Scholar]
  142. 142. 
    Machold RP, Wiertz EJ, Jones TR, Ploegh HL 1997. The HCMV gene products US11 and US2 differ in their ability to attack allelic forms of murine major histocompatibility complex (MHC) class I heavy chains. J. Exp. Med. 185:363–66
    [Google Scholar]
  143. 143. 
    Ahn K, Angulo A, Ghazal P, Peterson PA, Yang Y, Fruh K 1996. Human cytomegalovirus inhibits antigen presentation by a sequential multistep process. PNAS 93:10990–95
    [Google Scholar]
  144. 144. 
    Park B, Spooner E, Houser BL, Strominger JL, Ploegh HL 2010. The HCMV membrane glycoprotein US10 selectively targets HLA-G for degradation. J. Exp. Med. 207:2033–41
    [Google Scholar]
  145. 145. 
    Hansen SG, Powers CJ, Richards R, Ventura AB, Ford JC et al. 2010. Evasion of CD8+ T cells is critical for superinfection by cytomegalovirus. Science 328:102–6
    [Google Scholar]
  146. 146. 
    Wagner M, Gutermann A, Podlech J, Reddehase MJ, Koszinowski UH 2002. Major histocompatibility complex class I allele-specific cooperative and competitive interactions between immune evasion proteins of cytomegalovirus. J. Exp. Med. 196:805–16
    [Google Scholar]
  147. 147. 
    Ahn K, Gruhler A, Galocha B, Jones TR, Wiertz EJ et al. 1997. The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity 6:613–21
    [Google Scholar]
  148. 148. 
    Verweij MC, Horst D, Griffin BD, Luteijn RD, Davison AJ et al. 2015. Viral inhibition of the transporter associated with antigen processing (TAP): a striking example of functional convergent evolution. PLOS Pathog 11:e1004743
    [Google Scholar]
  149. 149. 
    Fruh K, Bartee E, Gouveia K, Mansouri M 2002. Immune evasion by a novel family of viral PHD/LAP-finger proteins of gamma-2 herpesviruses and poxviruses. Virus Res 88:55–69
    [Google Scholar]
  150. 150. 
    McCoy WH 4th, Wang X, Yokoyama WM, Hansen TH, Fremont DH 2013. Cowpox virus employs a two-pronged strategy to outflank MHCI antigen presentation. Mol. Immunol. 55:156–58
    [Google Scholar]
  151. 151. 
    Griffin BD, Gram AM, Mulder A, Van Leeuwen D, Claas FH et al. 2013. EBV BILF1 evolved to downregulate cell surface display of a wide range of HLA class I molecules through their cytoplasmic tail. J. Immunol. 190:1672–84
    [Google Scholar]
  152. 152. 
    Bottley G, Watherston OG, Hiew YL, Norrild B, Cook GP, Blair GE 2008. High-risk human papillomavirus E7 expression reduces cell-surface MHC class I molecules and increases susceptibility to natural killer cells. Oncogene 27:1794–99
    [Google Scholar]
  153. 153. 
    Babic M, Pyzik M, Zafirova B, Mitrovic M, Butorac V et al. 2010. Cytomegalovirus immunoevasin reveals the physiological role of “missing self” recognition in natural killer cell dependent virus control in vivo. J. Exp. Med. 207:2663–73
    [Google Scholar]
  154. 154. 
    Corbett AJ, Forbes CA, Moro D, Scalzo AA 2007. Extensive sequence variation exists among isolates of murine cytomegalovirus within members of the m02 family of genes. J. Gen. Virol. 88:758–69
    [Google Scholar]
  155. 155. 
    Desrosiers MP, Kielczewska A, Loredo-Osti JC, Adam SG, Makrigiannis AP et al. 2005. Epistasis between mouse Klra and major histocompatibility complex class I loci is associated with a new mechanism of natural killer cell-mediated innate resistance to cytomegalovirus infection. Nat. Genet. 37:593–99
    [Google Scholar]
  156. 156. 
    Kielczewska A, Pyzik M, Sun T, Krmpotic A, Lodoen MB et al. 2009. Ly49P recognition of cytomegalovirus-infected cells expressing H2-Dk and CMV-encoded m04 correlates with the NK cell antiviral response. J. Exp. Med. 206:515–23
    [Google Scholar]
  157. 157. 
    Pyzik M, Charbonneau B, Gendron-Pontbriand EM, Babic M, Krmpotic A et al. 2011. Distinct MHC class I-dependent NK cell-activating receptors control cytomegalovirus infection in different mouse strains. J. Exp. Med. 208:1105–17
    [Google Scholar]
  158. 158. 
    Glasner A, Oiknine-Djian E, Weisblum Y, Diab M, Panet A et al. 2017. Zika virus escapes NK cell detection by upregulating major histocompatibility complex class I molecules. J. Virol. 91:e00785-17
    [Google Scholar]
  159. 159. 
    Hershkovitz O, Zilka A, Bar-Ilan A, Abutbul S, Davidson A et al. 2008. Dengue virus replicon expressing the nonstructural proteins suffices to enhance membrane expression of HLA class I and inhibit lysis by human NK cells. J. Virol. 82:7666–76
    [Google Scholar]
  160. 160. 
    Momburg F, Mullbacher A, Lobigs M 2001. Modulation of transporter associated with antigen processing (TAP)-mediated peptide import into the endoplasmic reticulum by flavivirus infection. J. Virol. 75:5663–71
    [Google Scholar]
  161. 161. 
    Herzer K, Falk CS, Encke J, Eichhorst ST, Ulsenheimer A et al. 2003. Upregulation of major histocompatibility complex class I on liver cells by hepatitis C virus core protein via p53 and TAP1 impairs natural killer cell cytotoxicity. J. Virol. 77:8299–309
    [Google Scholar]
  162. 162. 
    Townsley E, O'Connor G, Cosgrove C, Woda M, Co M et al. 2016. Interaction of a dengue virus NS1-derived peptide with the inhibitory receptor KIR3DL1 on natural killer cells. Clin. Exp. Immunol. 183:419–30
    [Google Scholar]
  163. 163. 
    Orr MT, Wu J, Fang M, Sigal LJ, Spee P et al. 2010. Development and function of CD94-deficient natural killer cells. PLOS ONE 5:e15184
    [Google Scholar]
  164. 164. 
    Drews E, Adam A, Htoo P, Townsley E, Mathew A 2018. Upregulation of HLA-E by dengue and not Zika viruses. Clin. Transl. Immunol. 7:e1039
    [Google Scholar]
  165. 165. 
    Tomasec P, Braud VM, Rickards C, Powell MB, McSharry BP et al. 2000. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 287:1031–33
    [Google Scholar]
  166. 166. 
    Zhang C, Wang XM, Li SR, Twelkmeyer T, Wang WH et al. 2019. NKG2A is a NK cell exhaustion checkpoint for HCV persistence. Nat. Commun. 10:1507
    [Google Scholar]
  167. 167. 
    Nattermann J, Nischalke HD, Hofmeister V, Ahlenstiel G, Zimmermann H et al. 2005. The HLA-A2 restricted T cell epitope HCV core 35–44 stabilizes HLA-E expression and inhibits cytolysis mediated by natural killer cells. Am. J. Pathol. 166:443–53
    [Google Scholar]
  168. 168. 
    Heatley SL, Pietra G, Lin J, Widjaja JM, Harpur CM et al. 2013. Polymorphism in human cytomegalovirus UL40 impacts on recognition of human leukocyte antigen-E (HLA-E) by natural killer cells. J. Biol. Chem. 288:8679–90
    [Google Scholar]
  169. 169. 
    Hammer Q, Ruckert T, Borst EM, Dunst J, Haubner A et al. 2018. Peptide-specific recognition of human cytomegalovirus strains controls adaptive natural killer cells. Nat. Immunol. 19:453–63
    [Google Scholar]
  170. 170. 
    Wang X, Piersma SJ, Nelson CA, Dai YN, Christensen T et al. 2018. A herpesvirus encoded Qa-1 mimic inhibits natural killer cell cytotoxicity through CD94/NKG2A receptor engagement. eLife 7:e38667
    [Google Scholar]
  171. 171. 
    Yang Z, Bjorkman PJ. 2008. Structure of UL18, a peptide-binding viral MHC mimic, bound to a host inhibitory receptor. PNAS 105:10095–100
    [Google Scholar]
  172. 172. 
    Kaiser BK, Pizarro JC, Kerns J, Strong RK 2008. Structural basis for NKG2A/CD94 recognition of HLA-E. PNAS 105:6696–701
    [Google Scholar]
  173. 173. 
    Prod'homme V, Griffin C, Aicheler RJ, Wang EC, McSharry BP et al. 2007. The human cytomegalovirus MHC class I homolog UL18 inhibits LIR-1+ but activates LIR-1 NK cells. J. Immunol. 178:4473–81
    [Google Scholar]
  174. 174. 
    Prod'homme V, Tomasec P, Cunningham C, Lemberg MK, Stanton RJ et al. 2012. Human cytomegalovirus UL40 signal peptide regulates cell surface expression of the NK cell ligands HLA-E and gpUL18. J. Immunol. 188:2794–804
    [Google Scholar]
  175. 175. 
    Davidson CL, Li NL, Burshtyn DN 2010. LILRB1 polymorphism and surface phenotypes of natural killer cells. Hum. Immunol. 71:942–49
    [Google Scholar]
  176. 176. 
    Yu K, Davidson CL, Wojtowicz A, Lisboa L, Wang T et al. 2018. LILRB1 polymorphisms influence posttransplant HCMV susceptibility and ligand interactions. J. Clin. Investig. 128:1523–37
    [Google Scholar]
  177. 177. 
    Mans J, Natarajan K, Balbo A, Schuck P, Eikel D et al. 2007. Cellular expression and crystal structure of the murine cytomegalovirus major histocompatibility complex class I-like glycoprotein, m153. J. Biol. Chem. 282:35247–58
    [Google Scholar]
  178. 178. 
    Kubota A, Kubota S, Farrell HE, Davis-Poynter N, Takei F 1999. Inhibition of NK cells by murine CMV-encoded class I MHC homologue m144. Cell Immunol 191:145–51
    [Google Scholar]
  179. 179. 
    Farrell HE, Vally H, Lynch DM, Fleming P, Shellam GR et al. 1997. Inhibition of natural killer cells by a cytomegalovirus MHC class I homologue in vivo. Nature 386:510–14
    [Google Scholar]
  180. 180. 
    Natarajan K, Hicks A, Mans J, Robinson H, Guan R et al. 2006. Crystal structure of the murine cytomegalovirus MHC-I homolog m144. J. Mol. Biol. 358:157–71
    [Google Scholar]
  181. 181. 
    Smith HR, Heusel JW, Mehta IK, Kim S, Dorner BG et al. 2002. Recognition of a virus-encoded ligand by a natural killer cell activation receptor. PNAS 99:8826–31
    [Google Scholar]
  182. 182. 
    Arase H, Mocarski ES, Campbell AE, Hill AB, Lanier LL 2002. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296:1323–26
    [Google Scholar]
  183. 183. 
    Corbett AJ, Coudert JD, Forbes CA, Scalzo AA 2011. Functional consequences of natural sequence variation of murine cytomegalovirus m157 for Ly49 receptor specificity and NK cell activation. J. Immunol. 186:1713–22
    [Google Scholar]
  184. 184. 
    Brown MG, Dokun AO, Heusel JW, Smith HR, Beckman DL et al. 2001. Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science 292:934–37
    [Google Scholar]
  185. 185. 
    Lee SH, Girard S, Macina D, Busa M, Zafer A 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. 28:42–45
    [Google Scholar]
  186. 186. 
    French AR, Pingel JT, Wagner M, Bubic I, Yang L et al. 2004. Escape of mutant double-stranded DNA virus from innate immune control. Immunity 20:747–56
    [Google Scholar]
  187. 187. 
    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. 201:1319–32
    [Google Scholar]
  188. 188. 
    Adams EJ, Juo ZS, Venook RT, Boulanger MJ, Arase H et al. 2007. Structural elucidation of the m157 mouse cytomegalovirus ligand for Ly49 natural killer cell receptors. PNAS 104:10128–33
    [Google Scholar]
  189. 189. 
    Forbes CA, Scalzo AA, Degli-Esposti MA, Coudert JD 2014. Ly49C-dependent control of MCMV infection by NK cells is cis-regulated by MHC class I molecules. PLOS Pathog 10:e1004161
    [Google Scholar]
  190. 190. 
    Plougastel B, Matsumoto K, Dubbelde C, Yokoyama WM 2001. Analysis of a 1-Mb BAC contig overlapping the mouse Nkrp1 cluster of genes: cloning of three new Nkrp1 members, Nkrp1d, Nkrp1e, and Nkrp1f. Immunogenetics 53:592–98
    [Google Scholar]
  191. 191. 
    Carlyle JR, Mesci A, Ljutic B, Belanger S, Tai LH et al. 2006. Molecular and genetic basis for strain-dependent NK1.1 alloreactivity of mouse NK cells. J. Immunol. 176:7511–24
    [Google Scholar]
  192. 192. 
    Rosen DB, Cao W, Avery DT, Tangye SG, Liu YJ et al. 2008. Functional consequences of interactions between human NKR-P1A and its ligand LLT1 expressed on activated dendritic cells and B cells. J. Immunol. 180:6508–17
    [Google Scholar]
  193. 193. 
    Voigt S, Mesci A, Ettinger J, Fine JH, Chen P et al. 2007. Cytomegalovirus evasion of innate immunity by subversion of the NKR-P1B:Clr-b missing-self axis. Immunity 26:617–27
    [Google Scholar]
  194. 194. 
    Williams KJ, Wilson E, Davidson CL, Aguilar OA, Fu L et al. 2012. Poxvirus infection-associated downregulation of C-type lectin-related-b prevents NK cell inhibition by NK receptor protein-1B. J. Immunol. 188:4980–91
    [Google Scholar]
  195. 195. 
    Aguilar OA, Mesci A, Ma J, Chen P, Kirkham CL et al. 2015. Modulation of Clr ligand expression and NKR-P1 receptor function during murine cytomegalovirus infection. J. Innate Immun. 7:584–600
    [Google Scholar]
  196. 196. 
    Rahim MM, Wight A, Mahmoud AB, Aguilar OA, Lee SH et al. 2016. Expansion and protection by a virus-specific NK cell subset lacking expression of the inhibitory NKR-P1B receptor during murine cytomegalovirus infection. J. Immunol. 197:2325–37
    [Google Scholar]
  197. 197. 
    Aguilar OA, Berry R, Rahim MMA, Reichel JJ, Popovic B et al. 2017. A viral immunoevasin controls innate immunity by targeting the prototypical natural killer cell receptor family. Cell 169:58–71.e14
    [Google Scholar]
  198. 198. 
    Weizman OE, Song E, Adams NM, Hildreth AD, Riggan L et al. 2019. Mouse cytomegalovirus-experienced ILC1s acquire a memory response dependent on the viral glycoprotein m12. Nat. Immunol. 20:1004–11
    [Google Scholar]
  199. 199. 
    Ghasemi R, Lazear E, Wang X, Arefanian S, Zheleznyak A et al. 2016. Selective targeting of IL-2 to NKG2D bearing cells for improved immunotherapy. Nat. Commun. 7:12878
    [Google Scholar]
  200. 200. 
    Diamond MS. 2019. No IL-18BP? Avoid HAV. J. Exp. Med. 216:1728–29
    [Google Scholar]
  201. 201. 
    Gabay C, Fautrel B, Rech J, Spertini F, Feist E et al. 2018. Open-label, multicentre, dose-escalating phase II clinical trial on the safety and efficacy of tadekinig alfa (IL-18BP) in adult-onset Still's disease. Ann. Rheum. Dis. 77:840–47
    [Google Scholar]
  202. 202. 
    De Re V, Caggiari L, De Zorzi M, Repetto O, Zignego AL et al. 2015. Genetic diversity of the KIR/HLA system and susceptibility to hepatitis C virus-related diseases. PLOS ONE 10:e0117420
    [Google Scholar]
  203. 203. 
    Di Bona D, Scafidi V, Plaia A, Colomba C, Nuzzo D et al. 2014. HLA and killer cell immunoglobulin-like receptors influence the natural course of CMV infection. J. Infect. Dis. 210:1083–89
    [Google Scholar]
  204. 204. 
    Jiang Y, Chen O, Cui C, Zhao B, Han X et al. 2013. KIR3DS1/L1 and HLA-Bw4–80I are associated with HIV disease progression among HIV typical progressors and long-term nonprogressors. BMC Infect. Dis. 13:405
    [Google Scholar]
  205. 205. 
    Fadda L, Alter G. 2011. KIR/HLA: genetic clues for a role of NK cells in the control of HIV. Adv. Exp. Med. Biol. 780:27–36
    [Google Scholar]
  206. 206. 
    Albrecht C, Malzahn D, Brameier M, Hermes M, Ansari AA, Walter L 2014. Progression to AIDS in SIV-infected rhesus macaques is associated with distinct KIR and MHC class I polymorphisms and NK cell dysfunction. Front. Immunol. 5:600
    [Google Scholar]
  207. 207. 
    Ries M, Reynolds MR, Bashkueva K, Crosno K, Capuano S 3rd et al. 2017. KIR3DL01 upregulation on gut natural killer cells in response to SIV infection of KIR- and MHC class I-defined rhesus macaques. PLOS Pathog 13:e1006506
    [Google Scholar]
  208. 208. 
    Korner C, Simoneau CR, Schommers P, Granoff M, Ziegler M et al. 2017. HIV-1-mediated downmodulation of HLA-C impacts target cell recognition and antiviral activity of NK cells. Cell Host Microbe 22:111–19.e4
    [Google Scholar]
  209. 209. 
    Wauquier N, Petitdemange C, Tarantino N, Maucourant C, Coomber M et al. 2019. HLA-C-restricted viral epitopes are associated with an escape mechanism from KIR2DL2+ NK cells in Lassa virus infection. EBioMedicine 40:605–13
    [Google Scholar]
  210. 210. 
    Guma M, Angulo A, Vilches C, Gomez-Lozano N, Malats N, Lopez-Botet M 2004. Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood 104:3664–71
    [Google Scholar]
  211. 211. 
    Lee J, Zhang T, Hwang I, Kim A, Nitschke L et al. 2015. Epigenetic modification and antibody-dependent expansion of memory-like NK cells in human cytomegalovirus-infected individuals. Immunity 42:431–42
    [Google Scholar]
  212. 212. 
    Schlums H, Cichocki F, Tesi B, Theorell J, Beziat V et al. 2015. Cytomegalovirus infection drives adaptive epigenetic diversification of NK cells with altered signaling and effector function. Immunity 42:443–56
    [Google Scholar]
  213. 213. 
    Sharpe HR, Bowyer G, Brackenridge S, Lambe T 2019. HLA-E: exploiting pathogen-host interactions for vaccine development. Clin. Exp. Immunol. 196:167–77
    [Google Scholar]
  214. 214. 
    Hansen SG, Ford JC, Lewis MS, Ventura AB, Hughes CM et al. 2011. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 473:523–27
    [Google Scholar]
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