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  • 제24권4호
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  • Pages.29.1-29.18
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  • 2024
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  • 1598-2629(pISSN)
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  • 2092-6685(eISSN)
대한면역학회 (The Korean Association of Immunobiologists)
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The Multifaceted Roles of NK Cells in the Context of Murine Cytomegalovirus and Lymphocytic Choriomeningitis Virus Infections

  • Thamer A. Hamdan (Department of Basic Dental Sciences, Faculty of Dentistry, Al-Ahliyya Amman University)
  • 투고 : 2024.02.21
  • 심사 : 2024.06.03
  • 발행 : 2024.08.31
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초록

NK cells belong to innate lymphoid cells and able to eliminate infected cells and tumor cells. NK cells play a valuable role in controlling viral infections. Also, they have the potential to shape the adaptive immunity via a unique crosstalk with the different immune cells. Murine models are important tools for delineating the immunological phenomena in viral infection. To decipher the immunological virus-host interactions, two major infection models are being investigated in mice regarding NK cell-mediated recognition: murine cytomegalovirus (MCMV) and lymphocytic choriomeningitis virus (LCMV). In this review, we recapitulate recent findings regarding the multifaceted role of NK cells in controlling LCMV and MCMV infections and outline the exquisite interplay between NK cells and other immune cells in these two settings. Considering that, infections with MCMV and LCMV recapitulates many physiopathological characteristics of human cytomegalovirus infection and chronic virus infections respectively, this study will extend our understanding of NK cells biology in interactions between the virus and its natural host.

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참고문헌

  1. Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol 2008;9:503-510. https://doi.org/10.1038/ni1582
  2. Min-Oo G, Kamimura Y, Hendricks DW, Nabekura T, Lanier LL. Natural killer cells: walking three paths down memory lane. Trends Immunol 2013;34:251-258. https://doi.org/10.1016/j.it.2013.02.005
  3. Hammer Q, Ruckert T, Romagnani C. Natural killer cell specificity for viral infections. Nat Immunol 2018;19:800-808.
  4. Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol 1999;17:189-220. https://doi.org/10.1146/annurev.immunol.17.1.189
  5. Sandu I, Oxenius A. T-cell heterogeneity, progenitor-progeny relationships, and function during latent and chronic viral infections. Immunol Rev 2023;316:136-159. https://doi.org/10.1111/imr.13203
  6. Agnellini P, Wolint P, Rehr M, Cahenzli J, Karrer U, Oxenius A. Impaired NFAT nuclear translocation results in split exhaustion of virus-specific CD8+ T cell functions during chronic viral infection. Proc Natl Acad Sci U S A 2007;104:4565-4570. https://doi.org/10.1073/pnas.0610335104
  7. Mueller SN, Ahmed R. High antigen levels are the cause of T cell exhaustion during chronic viral infection. Proc Natl Acad Sci U S A 2009;106:8623-8628. https://doi.org/10.1073/pnas.0809818106
  8. Goodier MR, Jonjic S, Riley EM, Juranic Lisnic V. CMV and natural killer cells: shaping the response to vaccination. Eur J Immunol 2018;48:50-65. https://doi.org/10.1002/eji.201646762
  9. Krmpotic A, Bubic I, Polic B, Lucin P, Jonjic S. Pathogenesis of murine cytomegalovirus infection. Microbes Infect 2003;5:1263-1277.
  10. Mitrovic M, Arapovic J, Jordan S, Fodil-Cornu N, Ebert S, Vidal SM, Krmpotic A, Reddehase MJ, Jonjic S. The NK cell response to mouse cytomegalovirus infection affects the level and kinetics of the early CD8(+) T-cell response. J Virol 2012;86:2165-2175. https://doi.org/10.1128/JVI.06042-11
  11. Zangger N, Oderbolz J, Oxenius A. CD4 T cell-mediated immune control of cytomegalovirus infection in murine salivary glands. Pathogens 2021;10:1531.
  12. Studstill CJ, Hahm B. Chronic LCMV infection is fortified with versatile tactics to suppress host t cell immunity and establish viral persistence. Viruses 2021;13:1951.
  13. Caron L, Delisle JS, Strong JE, Deschambault Y, Lombard-Vadnais F, Labbe AC, Lesage S. Armstrong strain lymphocytic choriomeningitis virus infection after accidental laboratory exposure. Virol J 2023;20:294.
  14. Welsh RM, Waggoner SN. NK cells controlling virus-specific T cells: Rheostats for acute vs. persistent infections. Virology 2013;435:37-45. https://doi.org/10.1016/j.virol.2012.10.005
  15. Gatherer D, Depledge DP, Hartley CA, Szpara ML, Vaz PK, Benko M, Brandt CR, Bryant NA, Dastjerdi A, Doszpoly A, et al. ICTV virus taxonomy profile: Herpesviridae 2021. J Gen Virol 2021;102:001673.
  16. Hudson JB. The murine cytomegalovirus as a model for the study of viral pathogenesis and persistent infections. Arch Virol 1979;62:1-29. https://doi.org/10.1007/BF01314900
  17. Tang Q, Maul GG. Mouse cytomegalovirus crosses the species barrier with help from a few human cytomegalovirus proteins. J Virol 2006;80:7510-7521. https://doi.org/10.1128/JVI.00684-06
  18. Brune W, Hengel H, Koszinowski UH. A mouse model for cytomegalovirus infection.Curr Protoc Immunol 2001;Chapter 19:Unit 19.7.
  19. Rawlinson WD, Farrell HE, Barrell BG. Analysis of the complete DNA sequence of murine cytomegalovirus. J Virol 1996;70:8833-8849. https://doi.org/10.1128/jvi.70.12.8833-8849.1996
  20. Sitnik KM, Krstanovic F, Godecke N, Rand U, Kubsch T, Maass H, Kim Y, Brizic I, Cicin-Sain L. Fibroblasts are a site of murine cytomegalovirus lytic replication and Stat1-dependent latent persistence in vivo. Nat Commun 2023;14:3087.
  21. McNab F, Mayer-Barber K, Sher A, Wack A, O'Garra A. Type I interferons in infectious disease. Nat Rev Immunol 2015;15:87-103.
  22. Presti RM, Pollock JL, Dal Canto AJ, O'Guin AK, Virgin HW 4th. Interferon gamma regulates acute and latent murine cytomegalovirus infection and chronic disease of the great vessels. J Exp Med 1998;188:577-588. https://doi.org/10.1084/jem.188.3.577
  23. Gil MP, Bohn E, O'Guin AK, Ramana CV, Levine B, Stark GR, Virgin HW, Schreiber RD. Biologic consequences of Stat1-independent IFN signaling. Proc Natl Acad Sci U S A 2001;98:6680-6685. https://doi.org/10.1073/pnas.111163898
  24. Hoffmann HH, Schneider WM, Rice CM. Interferons and viruses: an evolutionary arms race of molecular interactions. Trends Immunol 2015;36:124-138. https://doi.org/10.1016/j.it.2015.01.004
  25. Lazear HM, Nice TJ, Diamond MS. Interferon-λ: immune functions at barrier surfaces and beyond. Immunity 2015;43:15-28. https://doi.org/10.1016/j.immuni.2015.07.001
  26. Billiau A, Matthys P. Interferon-gamma: a historical perspective. Cytokine Growth Factor Rev 2009;20:97-113. https://doi.org/10.1016/j.cytogfr.2009.02.004
  27. McKenzie AN, Spits H, Eberl G. Innate lymphoid cells in inflammation and immunity. Immunity 2014;41:366-374. https://doi.org/10.1016/j.immuni.2014.09.006
  28. Schroder K, Hertzog PJ, Ravasi T, Hume DA. Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 2004;75:163-189. https://doi.org/10.1189/jlb.0603252
  29. Kang S, Brown HM, Hwang S. Direct antiviral mechanisms of interferon-gamma. Immune Netw 2018;18:e33.
  30. Kropp KA, Robertson KA, Sing G, Rodriguez-Martin S, Blanc M, Lacaze P, Hassim MF, Khondoker MR, Busche A, Dickinson P, et al. Reversible inhibition of murine cytomegalovirus replication by gamma interferon (IFN-γ) in primary macrophages involves a primed type I IFN-signaling subnetwork for full establishment of an immediate-early antiviral state. J Virol 2011;85:10286-10299. https://doi.org/10.1128/JVI.00373-11
  31. Heise MT, Virgin HW 4th. The T-cell-independent role of gamma interferon and tumor necrosis factor alpha in macrophage activation during murine cytomegalovirus and herpes simplex virus infections. J Virol 1995;69:904-909. https://doi.org/10.1128/jvi.69.2.904-909.1995
  32. Gribaudo G, Ravaglia S, Caliendo A, Cavallo R, Gariglio M, Martinotti MG, Landolfo S. Interferons inhibit onset of murine cytomegalovirus immediate-early gene transcription. Virology 1993;197:303-311. https://doi.org/10.1006/viro.1993.1591
  33. Lucin P, Jonjic S, Messerle M, Polic B, Hengel H, Koszinowski UH. Late phase inhibition of murine cytomegalovirus replication by synergistic action of interferon-gamma and tumour necrosis factor. J Gen Virol 1994;75:101-110.
  34. Senik A, Stefanos S, Kolb JP, Lucero M, Falcoff E. Enhancement of mouse natural killer cell activity by type II interferon. Ann Immunol (Paris) 1980;131C:349-361.
  35. Nathan CF, Murray HW, Wiebe ME, Rubin BY. Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J Exp Med 1983;158:670-689. https://doi.org/10.1084/jem.158.3.670
  36. Leibson HJ, Gefter M, Zlotnik A, Marrack P, Kappler JW. Role of gamma-interferon in antibody-producing responses. Nature 1984;309:799-801. https://doi.org/10.1038/309799a0
  37. Gajewski TF, Fitch FW. Anti-proliferative effect of IFN-gamma in immune regulation. I. IFN-gamma inhibits the proliferation of Th2 but not Th1 murine helper T lymphocyte clones. J Immunol 1988;140:4245-4252. https://doi.org/10.4049/jimmunol.140.12.4245
  38. Hengel H, Lucin P, Jonjic S, Ruppert T, Koszinowski UH. Restoration of cytomegalovirus antigen presentation by gamma interferon combats viral escape. J Virol 1994;68:289-297. https://doi.org/10.1128/jvi.68.1.289-297.1994
  39. Brown MG, Dokun AO, Heusel JW, Smith HR, Beckman DL, Blattenberger EA, Dubbelde CE, Stone LR, Scalzo AA, Yokoyama WM. Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science 2001;292:934-937. https://doi.org/10.1126/science.1060042
  40. Scalzo AA, Corbett AJ, Rawlinson WD, Scott GM, Degli-Esposti MA. The interplay between host and viral factors in shaping the outcome of cytomegalovirus infection. Immunol Cell Biol 2007;85:46-54. https://doi.org/10.1038/sj.icb.7100013
  41. Lee SH, Miyagi T, Biron CA. Keeping NK cells in highly regulated antiviral warfare. Trends Immunol 2007;28:252-259.
  42. Arase H, Mocarski ES, Campbell AE, Hill AB, Lanier LL. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 2002;296:1323-1326. https://doi.org/10.1126/science.1070884
  43. Bubic I, Wagner M, Krmpotic A, Saulig T, Kim S, Yokoyama WM, Jonjic S, Koszinowski UH. Gain of virulence caused by loss of a gene in murine cytomegalovirus. J Virol 2004;78:7536-7544. https://doi.org/10.1128/JVI.78.14.7536-7544.2004
  44. Lanier LL. DAP10- and DAP12-associated receptors in innate immunity. Immunol Rev 2009;227:150-160. https://doi.org/10.1111/j.1600-065X.2008.00720.x
  45. Nabekura T, Lanier LL. Antigen-specific expansion and differentiation of natural killer cells by alloantigen stimulation. J Exp Med 2014;211:2455-2465. https://doi.org/10.1084/jem.20140798
  46. Orr MT, Sun JC, Hesslein DG, Arase H, Phillips JH, Takai T, Lanier LL. Ly49H signaling through DAP10 is essential for optimal natural killer cell responses to mouse cytomegalovirus infection. J Exp Med 2009;206:807-817. https://doi.org/10.1084/jem.20090168
  47. Sun JC, Beilke JN, Lanier LL. Adaptive immune features of natural killer cells. Nature 2009;457:557-561. https://doi.org/10.1038/nature07665
  48. Dokun AO, Kim S, Smith HR, Kang HS, Chu DT, Yokoyama WM. Specific and nonspecific NK cell activation during virus infection. Nat Immunol 2001;2:951-956. https://doi.org/10.1038/ni714
  49. Terren I, Orrantia A, Astarloa-Pando G, Amarilla-Irusta A, Zenarruzabeitia O, Borrego F. Cytokine-induced memory-like NK cells: from the basics to clinical applications. Front Immunol 2022;13:884648.
  50. Sun JC, Ma A, Lanier LL. Cutting edge: IL-15-independent NK cell response to mouse cytomegalovirus infection. J Immunol 2009;183:2911-2914. https://doi.org/10.4049/jimmunol.0901872
  51. Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 2003;3:133-146.
  52. Sun JC, Madera S, Bezman NA, Beilke JN, Kaplan MH, Lanier LL. Proinflammatory cytokine signaling required for the generation of natural killer cell memory. J Exp Med 2012;209:947-954. https://doi.org/10.1084/jem.20111760
  53. Zeleznjak J, Popovic B, Krmpotic A, Jonjic S, Lisnic VJ. Mouse cytomegalovirus encoded immunoevasins and evolution of Ly49 receptors - sidekicks or enemies? Immunol Lett 2017;189:40-47. https://doi.org/10.1016/j.imlet.2017.04.007
  54. Corbett AJ, Coudert JD, Forbes CA, Scalzo AA. Functional consequences of natural sequence variation of murine cytomegalovirus m157 for Ly49 receptor specificity and NK cell activation. J Immunol 2011;186:1713-1722.
  55. Robbins SH, Bessou G, Cornillon A, Zucchini N, Rupp B, Ruzsics Z, Sacher T, Tomasello E, Vivier E, Koszinowski UH, et al. Natural killer cells promote early CD8 T cell responses against cytomegalovirus. PLoS Pathog 2007;3:e123.
  56. Asselin-Paturel C, Brizard G, Pin JJ, Briere F, Trinchieri G. Mouse strain differences in plasmacytoid dendritic cell frequency and function revealed by a novel monoclonal antibody. J Immunol 2003;171:6466-6477. https://doi.org/10.4049/jimmunol.171.12.6466
  57. Shibuya A, Campbell D, Hannum C, Yssel H, Franz-Bacon K, McClanahan T, Kitamura T, Nicholl J, Sutherland GR, Lanier LL, et al. DNAM-1, a novel adhesion molecule involved in the cytolytic function of T lymphocytes. Immunity 1996;4:573-581. https://doi.org/10.1016/S1074-7613(00)70060-4
  58. Nabekura T, Kanaya M, Shibuya A, Fu G, Gascoigne NR, Lanier LL. Costimulatory molecule DNAM-1 is essential for optimal differentiation of memory natural killer cells during mouse cytomegalovirus infection. Immunity 2014;40:225-234. https://doi.org/10.1016/j.immuni.2013.12.011
  59. Wu J, Song Y, Bakker AB, Bauer S, Spies T, Lanier LL, Phillips JH. An activating immunoreceptor complex formed by NKG2D and DAP10. Science 1999;285:730-732. https://doi.org/10.1126/science.285.5428.730
  60. Champsaur M, Lanier LL. Effect of NKG2D ligand expression on host immune responses. Immunol Rev 2010;235:267-285.
  61. Jamieson AM, Diefenbach A, McMahon CW, Xiong N, Carlyle JR, Raulet DH. The role of the NKG2D immunoreceptor in immune cell activation and natural killing. Immunity 2002;17:19-29. https://doi.org/10.1016/S1074-7613(02)00333-3
  62. Raulet DH. Roles of the NKG2D immunoreceptor and its ligands. Nat Rev Immunol 2003;3:781-790. https://doi.org/10.1038/nri1199
  63. Diefenbach A, Tomasello E, Lucas M, Jamieson AM, Hsia JK, Vivier E, Raulet DH. Selective associations with signaling proteins determine stimulatory versus costimulatory activity of NKG2D. Nat Immunol 2002;3:1142-1149.
  64. Gilfillan S, Ho EL, Cella M, Yokoyama WM, Colonna M. NKG2D recruits two distinct adapters to trigger NK cell activation and costimulation. Nat Immunol 2002;3:1150-1155. https://doi.org/10.1038/ni857
  65. Billadeau DD, Upshaw JL, Schoon RA, Dick CJ, Leibson PJ. NKG2D-DAP10 triggers human NK cell-mediated killing via a Syk-independent regulatory pathway. Nat Immunol 2003;4:557-564. https://doi.org/10.1038/ni929
  66. Zompi S, Hamerman JA, Ogasawara K, Schweighoffer E, Tybulewicz VL, Di Santo JP, Lanier LL, Colucci F. NKG2D triggers cytotoxicity in mouse NK cells lacking DAP12 or Syk family kinases. Nat Immunol 2003;4:565-572.
  67. Nabekura T, Gotthardt D, Niizuma K, Trsan T, Jenus T, Jonjic S, Lanier LL. Cutting edge: NKG2D signaling enhances NK cell responses but alone is insufficient to drive expansion during mouse cytomegalovirus infection. J Immunol 2017;199:1567-1571. https://doi.org/10.4049/jimmunol.1700799
  68. Zafirova B, Mandaric S, Antulov R, Krmpotic A, Jonsson H, Yokoyama WM, Jonjic S, Polic B. Altered NK cell development and enhanced NK cell-mediated resistance to mouse cytomegalovirus in NKG2D-deficient mice. Immunity 2009;31:270-282. https://doi.org/10.1016/j.immuni.2009.06.017
  69. French AR, Sjolin H, Kim S, Koka R, Yang L, Young DA, Cerboni C, Tomasello E, Ma A, Vivier E, et al. DAP12 signaling directly augments proproliferative cytokine stimulation of NK cells during viral infections. J Immunol 2006;177:4981-4990. https://doi.org/10.4049/jimmunol.177.8.4981
  70. Ho EL, Carayannopoulos LN, Poursine-Laurent J, Kinder J, Plougastel B, Smith HR, Yokoyama WM. Costimulation of multiple NK cell activation receptors by NKG2D. J Immunol 2002;169:3667-3675. https://doi.org/10.4049/jimmunol.169.7.3667
  71. Jelencic V, Sestan M, Kavazovic I, Lenartic M, Marinovic S, Holmes TD, Prchal-Murphy M, Lisnic B, Sexl V, Bryceson YT, et al. NK cell receptor NKG2D sets activation threshold for the NCR1 receptor early in NK cell development. Nat Immunol 2018;19:1083-1092. https://doi.org/10.1038/s41590-018-0209-9
  72. Khan AU, Ali AK, Marr B, Jo D, Ahmadvand S, Fong-McMaster C, Almutairi SM, Wang L, Sad S, Harper ME, et al. The TNFα/TNFR2 axis mediates natural killer cell proliferation by promoting aerobic glycolysis. Cell Mol Immunol 2023;20:1140-1155.
  73. Huntington ND. Ironman training for NK cells. Nat Immunol 2023;24:1599-1601.
  74. Sheppard S, Schuster IS, Andoniou CE, Cocita C, Adejumo T, Kung SK, Sun JC, Degli-Esposti MA, Guerra N. The murine natural cytotoxic receptor NKp46/NCR1 controls TRAIL protein expression in NK cells and ILC1s. Cell Reports 2018;22:3385-3392. https://doi.org/10.1016/j.celrep.2018.03.023
  75. Pessino A, Sivori S, Bottino C, Malaspina A, Morelli L, Moretta L, Biassoni R, Moretta A. Molecular cloning of NKp46: a novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity. J Exp Med 1998;188:953-960. https://doi.org/10.1084/jem.188.5.953
  76. Biassoni R, Pessino A, Bottino C, Pende D, Moretta L, Moretta A. The murine homologue of the human NKp46, a triggering receptor involved in the induction of natural cytotoxicity. Eur J Immunol 1999;29:1014-1020. https://doi.org/10.1002/(SICI)1521-4141(199903)29:03<1014::AID-IMMU1014>3.0.CO;2-O
  77. Narni-Mancinelli E, Jaeger BN, Bernat C, Fenis A, Kung S, De Gassart A, Mahmood S, Gut M, Heath SC, Estelle J, et al. Tuning of natural killer cell reactivity by NKp46 and Helios calibrates T cell responses. Science 2012;335:344-348. https://doi.org/10.1126/science.1215621
  78. Walton SM, Mandaric S, Torti N, Zimmermann A, Hengel H, Oxenius A. Absence of cross-presenting cells in the salivary gland and viral immune evasion confine cytomegalovirus immune control to effector CD4 T cells. PLoS Pathog 2011;7:e1002214.
  79. Campbell AE, Cavanaugh VJ, Slater JS. The salivary glands as a privileged site of cytomegalovirus immune evasion and persistence. Med Microbiol Immunol (Berl) 2008;197:205-213. https://doi.org/10.1007/s00430-008-0077-2
  80. Nabekura T, Girard JP, Lanier LL. IL-33 receptor ST2 amplifies the expansion of NK cells and enhances host defense during mouse cytomegalovirus infection. J Immunol 2015;194:5948-5952. https://doi.org/10.4049/jimmunol.1500424
  81. Madera S, Sun JC. Cutting edge: stage-specific requirement of IL-18 for antiviral NK cell expansion. J Immunol 2015;194:1408-1412.
  82. French AR, Yokoyama WM. Natural killer cells and viral infections. Curr Opin Immunol 2003;15:45-51. https://doi.org/10.1016/S095279150200002X
  83. Hangartner L, Zinkernagel RM, Hengartner H. Antiviral antibody responses: the two extremes of a wide spectrum. Nat Rev Immunol 2006;6:231-243. https://doi.org/10.1038/nri1783
  84. Bukowski JF, Woda BA, Welsh RM. Pathogenesis of murine cytomegalovirus infection in natural killer cell-depleted mice. J Virol 1984;52:119-128. https://doi.org/10.1128/jvi.52.1.119-128.1984
  85. Halenius A, Gerke C, Hengel H. Classical and non-classical MHC I molecule manipulation by human cytomegalovirus: so many targets-but how many arrows in the quiver? Cell Mol Immunol 2015;12:139-153. https://doi.org/10.1038/cmi.2014.105
  86. Lisnic B, Lisnic VJ, Jonjic S. NK cell interplay with cytomegaloviruses. Curr Opin Virol 2015;15:9-18. https://doi.org/10.1016/j.coviro.2015.07.001
  87. Babic M, Pyzik M, Zafirova B, Mitrovic M, Butorac V, Lanier LL, Krmpotic A, Vidal SM, Jonjic S. Cytomegalovirus immunoevasin reveals the physiological role of "missing self " recognition in natural killer cell dependent virus control in vivo. J Exp Med 2010;207:2663-2673. https://doi.org/10.1084/jem.20100921
  88. Kavanagh DG, Gold MC, Wagner M, Koszinowski UH, Hill AB. The multiple immune-evasion genes of murine cytomegalovirus are not redundant: m4 and m152 inhibit antigen presentation in a complementary and cooperative fashion. J Exp Med 2001;194:967-978. https://doi.org/10.1084/jem.194.7.967
  89. Arapovic J, Lenac Rovis T, Reddy AB, Krmpotic A, Jonjic S. Promiscuity of MCMV immunoevasin of NKG2D: m138/fcr-1 down-modulates RAE-1epsilon in addition to MULT-1 and H60. Mol Immunol 2009;47:114-122.
  90. Lis N, Hein Z, Ghanwat SS, Ramnarayan VR, Chambers BJ, Springer S. The murine cytomegalovirus immunoevasin gp40/m152 inhibits NKG2D receptor RAE-1γ by intracellular retention and cell surface masking. J Cell Sci 2021;134:jcs257428.
  91. Jonjic S, Babic M, Polic B, Krmpotic A. Immune evasion of natural killer cells by viruses. Curr Opin Immunol 2008;20:30-38. https://doi.org/10.1097/MOP.0b013e3282f35f19
  92. Arnon TI, Achdout H, Levi O, Markel G, Saleh N, Katz G, Gazit R, Gonen-Gross T, Hanna J, Nahari E, et al. Inhibition of the NKp30 activating receptor by pp65 of human cytomegalovirus. Nat Immunol 2005;6:515-523.
  93. Sylwester AW, Mitchell BL, Edgar JB, Taormina C, Pelte C, Ruchti F, Sleath PR, Grabstein KH, Hosken NA, Kern F, et al. Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ T cells dominate the memory compartments of exposed subjects. J Exp Med 2005;202:673-685. https://doi.org/10.1084/jem.20050882
  94. Blees A, Januliene D, Hofmann T, Koller N, Schmidt C, Trowitzsch S, Moeller A, Tampe R. Structure of the human MHC-I peptide-loading complex. Nature 2017;551:525-528. https://doi.org/10.1038/nature24627
  95. Manandhar T, Ho GT, Pump WC, Blasczyk R, Bade-Doeding C. Battle between host immune cellular responses and HCMV immune evasion. Int J Mol Sci 2019;20:3626.
  96. Biron CA, Byron KS, Sullivan JL. Severe herpesvirus infections in an adolescent without natural killer cells. N Engl J Med 1989;320:1731-1735. https://doi.org/10.1056/NEJM198906293202605
  97. Orange JS. Natural killer cell deficiency. J Allergy Clin Immunol 2013;132:515-525. https://doi.org/10.1016/j.jaci.2013.07.020
  98. Oldstone MB, Ahmed R, Byrne J, Buchmeier MJ, Riviere Y, Southern P. Virus and immune responses: lymphocytic choriomeningitis virus as a prototype model of viral pathogenesis. Br Med Bull 1985;41:70-74. https://doi.org/10.1093/oxfordjournals.bmb.a072029
  99. Bonthius DJ. Lymphocytic choriomeningitis virus: an underrecognized cause of neurologic disease in the fetus, child, and adult. Semin Pediatr Neurol 2012;19:89-95. https://doi.org/10.1016/j.spen.2012.02.002
  100. Biggar RJ, Woodall JP, Walter PD, Haughie GE. Lymphocytic choriomeningitis outbreak associated with pet hamsters. Fifty-seven cases from New York State. JAMA 1975;232:494-500. https://doi.org/10.1001/jama.1975.03250050016009
  101. Zhou X, Ramachandran S, Mann M, Popkin DL. Role of lymphocytic choriomeningitis virus (LCMV) in understanding viral immunology: past, present and future. Viruses 2012;4:2650-2669. https://doi.org/10.3390/v4112650
  102. Welsh RM, Seedhom MO. Lymphocytic choriomeningitis virus (LCMV): propagation, quantitation, and storage.Curr Protoc Microbiol 2008;Chapter 15:Unit 15A.1.
  103. Emonet SF, de la Torre JC, Domingo E, Sevilla N. Arenavirus genetic diversity and its biological implications. Infect Genet Evol 2009;9:417-429. https://doi.org/10.1016/j.meegid.2009.03.005
  104. Lee KJ, Novella IS, Teng MN, Oldstone MB, de La Torre JC. NP and L proteins of lymphocytic choriomeningitis virus (LCMV) are sufficient for efficient transcription and replication of LCMV genomic RNA analogs. J Virol 2000;74:3470-3477. https://doi.org/10.1128/JVI.74.8.3470-3477.2000
  105. Vilibic-Cavlek T, Savic V, Ferenc T, Mrzljak A, Barbic L, Bogdanic M, Stevanovic V, Tabain I, Ferencak I, Zidovec-Lepej S. Lymphocytic choriomeningitis-emerging trends of a neglected virus: a narrative review. Trop Med Infect Dis 2021;6:88.
  106. Norris BA, Uebelhoer LS, Nakaya HI, Price AA, Grakoui A, Pulendran B. Chronic but not acute virus infection induces sustained expansion of myeloid suppressor cell numbers that inhibit viral-specific T cell immunity. Immunity 2013;38:309-321. https://doi.org/10.1016/j.immuni.2012.10.022
  107. Cao W, Henry MD, Borrow P, Yamada H, Elder JH, Ravkov EV, Nichol ST, Compans RW, Campbell KP, Oldstone MB. Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 1998;282:2079-2081. https://doi.org/10.1126/science.282.5396.2079
  108. Meyer BJ, de la Torre JC, Southern PJ. Arenaviruses: genomic RNAs, transcription, and replication. Curr Top Microbiol Immunol 2002;262:139-157.
  109. Takagi T, Ohsawa M, Morita C, Sato H, Ohsawa K. Genomic analysis and pathogenic characteristics of lymphocytic choriomeningitis virus strains isolated in Japan. Comp Med 2012;62:185-192.
  110. Dangi T, Chung YR, Palacio N, Penaloza-MacMaster P. Interrogating adaptive immunity using LCMV. Curr Protoc Immunol 2020;130:e99.
  111. Sevilla N, Kunz S, Holz A, Lewicki H, Homann D, Yamada H, Campbell KP, de La Torre JC, Oldstone MB. Immunosuppression and resultant viral persistence by specific viral targeting of dendritic cells. J Exp Med 2000;192:1249-1260. https://doi.org/10.1084/jem.192.9.1249
  112. Cook KD, Waggoner SN, Whitmire JK. NK cells and their ability to modulate T cells during virus infections. Crit Rev Immunol 2014;34:359-388. https://doi.org/10.1615/CritRevImmunol.2014010604
  113. Mempel TR, Henrickson SE, Von Andrian UH. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 2004;427:154-159. https://doi.org/10.1038/nature02238
  114. Walzer T, Dalod M, Robbins SH, Zitvogel L, Vivier E. Natural-killer cells and dendritic cells: "l'union fait la force". Blood 2005;106:2252-2258.
  115. Sivori S, Falco M, Della Chiesa M, Carlomagno S, Vitale M, Moretta L, Moretta A. CpG and double-stranded RNA trigger human NK cells by Toll-like receptors: induction of cytokine release and cytotoxicity against tumors and dendritic cells. Proc Natl Acad Sci U S A 2004;101:10116-10121. https://doi.org/10.1073/pnas.0403744101
  116. Biron CA, Nguyen KB, Pien GC. Innate immune responses to LCMV infections: natural killer cells and cytokines. Curr Top Microbiol Immunol 2002;263:7-27.
  117. Vivier E, Nunes JA, Vely F. Natural killer cell signaling pathways. Science 2004;306:1517-1519. https://doi.org/10.1126/science.1103478
  118. Bukowski JF, Woda BA, Habu S, Okumura K, Welsh RM. Natural killer cell depletion enhances virus synthesis and virus-induced hepatitis in vivo. J Immunol 1983;131:1531-1538. https://doi.org/10.4049/jimmunol.131.3.1531
  119. Welsh RM, O'Donnell CL, Shultz LD. Antiviral activity of NK 1.1+ natural killer cells in C57BL/6 scid mice infected with murine cytomegalovirus. Nat Immun 1994;13:239-245.
  120. Waggoner SN, Reighard SD, Gyurova IE, Cranert SA, Mahl SE, Karmele EP, McNally JP, Moran MT, Brooks TR, Yaqoob F, et al. Roles of natural killer cells in antiviral immunity. Curr Opin Virol 2016;16:15-23. https://doi.org/10.1016/j.coviro.2015.10.008
  121. Zhou J, Peng H, Li K, Qu K, Wang B, Wu Y, Ye L, Dong Z, Wei H, Sun R, et al. Liver-resident NK cells control antiviral activity of hepatic T cells via the PD-1-PD-L1 axis. Immunity 2019;50:403-417.e4. https://doi.org/10.1016/j.immuni.2018.12.024
  122. Lang PA, Lang KS, Xu HC, Grusdat M, Parish IA, Recher M, Elford AR, Dhanji S, Shaabani N, Tran CW, et al. Natural killer cell activation enhances immune pathology and promotes chronic infection by limiting CD8+ T-cell immunity. Proc Natl Acad Sci U S A 2012;109:1210-1215. https://doi.org/10.1073/pnas.1118834109
  123. Hamdan TA, Lang PA, Lang KS. The diverse functions of the ubiquitous Fcγ receptors and their unique constituent, FcRγ subunit. Pathogens 2020;9:140.
  124. Duhan V, Hamdan TA, Xu HC, Shinde P, Bhat H, Li F, Al-Matary Y, Haussinger D, Bezgovsek J, Friedrich SK, et al. NK cell-intrinsic FcεRIγ limits CD8+ T-cell expansion and thereby turns an acute into a chronic viral infection. PLoS Pathog 2019;15:e1007797.
  125. Pallmer K, Barnstorf I, Baumann NS, Borsa M, Jonjic S, Oxenius A. NK cells negatively regulate CD8 T cells via natural cytotoxicity receptor (NCR) 1 during LCMV infection. PLoS Pathog 2019;15:e1007725.
  126. Waggoner SN, Cornberg M, Selin LK, Welsh RM. Natural killer cells act as rheostats modulating antiviral T cells. Nature 2011;481:394-398.
  127. Waggoner SN, Taniguchi RT, Mathew PA, Kumar V, Welsh RM. Absence of mouse 2B4 promotes NK cell-mediated killing of activated CD8+ T cells, leading to prolonged viral persistence and altered pathogenesis. J Clin Invest 2010;120:1925-1938. https://doi.org/10.1172/JCI41264
  128. Cook KD, Whitmire JK. The depletion of NK cells prevents T cell exhaustion to efficiently control disseminating virus infection. J Immunol 2013;190:641-649. https://doi.org/10.4049/jimmunol.1202448
  129. Cook KD, Kline HC, Whitmire JK. NK cells inhibit humoral immunity by reducing the abundance of CD4+ T follicular helper cells during a chronic virus infection. J Leukoc Biol 2015;98:153-162. https://doi.org/10.1189/jlb.4HI1214-594R
  130. Mack EA, Kallal LE, Demers DA, Biron CA. Type 1 interferon induction of natural killer cell gamma interferon production for defense during lymphocytic choriomeningitis virus infection. MBio 2011;2:e00169-11.
  131. Madera S, Rapp M, Firth MA, Beilke JN, Lanier LL, Sun JC. Type I IFN promotes NK cell expansion during viral infection by protecting NK cells against fratricide. J Exp Med 2016;213:225-233. https://doi.org/10.1084/jem.20150712
  132. Crouse J, Bedenikovic G, Wiesel M, Ibberson M, Xenarios I, Von Laer D, Kalinke U, Vivier E, Jonjic S, Oxenius A. Type I interferons protect T cells against NK cell attack mediated by the activating receptor NCR1. Immunity 2014;40:961-973. https://doi.org/10.1016/j.immuni.2014.05.003
  133. Xu HC, Grusdat M, Pandyra AA, Polz R, Huang J, Sharma P, Deenen R, Kohrer K, Rahbar R, Diefenbach A, et al. Type I interferon protects antiviral CD8+ T cells from NK cell cytotoxicity. Immunity 2014;40:949-960. https://doi.org/10.1016/j.immuni.2014.05.004
  134. Huang Z, Kang SG, Li Y, Zak J, Shaabani N, Deng K, Shepherd J, Bhargava R, Teijaro JR, Xiao C. IFNAR1 signaling in NK cells promotes persistent virus infection. Sci Adv 2021;7:eabb8087.
  135. Rydyznski C, Daniels KA, Karmele EP, Brooks TR, Mahl SE, Moran MT, Li C, Sutiwisesak R, Welsh RM, Waggoner SN. Generation of cellular immune memory and B-cell immunity is impaired by natural killer cells. Nat Commun 2015;6:6375.
  136. Cardoso Alves L, Berger MD, Koutsandreas T, Kirschke N, Lauer C, Sporri R, Chatziioannou A, Corazza N, Krebs P. Non-apoptotic TRAIL function modulates NK cell activity during viral infection. EMBO Rep 2020;21:e48789.
  137. Pratumchai I, Zak J, Huang Z, Min B, Oldstone MB, Teijaro JR. B cell-derived IL-27 promotes control of persistent LCMV infection. Proc Natl Acad Sci U S A 2022;119:e2116741119.
  138. Butz EA, Bevan MJ. Massive expansion of antigen-specific CD8+ T cells during an acute virus infection. Immunity 1998;8:167-175. https://doi.org/10.1016/S1074-7613(00)80469-0
  139. Wherry EJ, Teichgraber V, Becker TC, Masopust D, Kaech SM, Antia R, von Andrian UH, Ahmed R. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol 2003;4:225-234.
  140. Wherry EJ, Blattman JN, Murali-Krishna K, van der Most R, Ahmed R. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J Virol 2003;77:4911-4927.
  141. Cornberg M, Kenney LL, Chen AT, Waggoner SN, Kim SK, Dienes HP, Welsh RM, Selin LK. Clonal exhaustion as a mechanism to protect against severe immunopathology and death from an overwhelming CD8 T cell response. Front Immunol 2013;4:475.
  142. Moskophidis D, Lechner F, Pircher H, Zinkernagel RM. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature 1993;362:758-761. https://doi.org/10.1038/362758a0
  143. Wherry EJ. T cell exhaustion. Nat Immunol 2011;12:492-499. https://doi.org/10.1038/ni.2035
  144. Lee SH, Kim KS, Fodil-Cornu N, Vidal SM, Biron CA. Activating receptors promote NK cell expansion for maintenance, IL-10 production, and CD8 T cell regulation during viral infection. J Exp Med 2009;206:2235-2251. https://doi.org/10.1084/jem.20082387
  145. Su HC, Orange JS, Fast LD, Chan AT, Simpson SJ, Terhorst C, Biron CA. IL-2-dependent NK cell responses discovered in virus-infected beta 2-microglobulin-deficient mice. J Immunol 1994;153:5674-5681. https://doi.org/10.4049/jimmunol.153.12.5674
  146. Whitmire JK, Eam B, Benning N, Whitton JL. Direct interferon-gamma signaling dramatically enhances CD4+ and CD8+ T cell memory. J Immunol 2007;179:1190-1197. https://doi.org/10.4049/jimmunol.179.2.1190
  147. Whitmire JK, Tan JT, Whitton JL. Interferon-gamma acts directly on CD8+ T cells to increase their abundance during virus infection. J Exp Med 2005;201:1053-1059. https://doi.org/10.1084/jem.20041463
  148. Whitmire JK, Benning N, Whitton JL. Cutting edge: early IFN-gamma signaling directly enhances primary antiviral CD4+ T cell responses. J Immunol 2005;175:5624-5628. https://doi.org/10.4049/jimmunol.175.9.5624
  149. Gerosa F, Baldani-Guerra B, Nisii C, Marchesini V, Carra G, Trinchieri G. Reciprocal activating interaction between natural killer cells and dendritic cells. J Exp Med 2002;195:327-333. https://doi.org/10.1084/jem.20010938
  150. Mocikat R, Braumuller H, Gumy A, Egeter O, Ziegler H, Reusch U, Bubeck A, Louis J, Mailhammer R, Riethmuller G, et al. Natural killer cells activated by MHC class I(low) targets prime dendritic cells to induce protective CD8 T cell responses. Immunity 2003;19:561-569. https://doi.org/10.1016/S1074-7613(03)00264-4
  151. Adam C, King S, Allgeier T, Braumuller H, Luking C, Mysliwietz J, Kriegeskorte A, Busch DH, Rocken M, Mocikat R. DC-NK cell cross talk as a novel CD4+ T-cell-independent pathway for antitumor CTL induction. Blood 2005;106:338-344.
  152. Andrews DM, Andoniou CE, Granucci F, Ricciardi-Castagnoli P, Degli-Esposti MA. Infection of dendritic cells by murine cytomegalovirus induces functional paralysis. Nat Immunol 2001;2:1077-1084. https://doi.org/10.1038/ni724
  153. Andrews DM, Estcourt MJ, Andoniou CE, Wikstrom ME, Khong A, Voigt V, Fleming P, Tabarias H, Hill GR, van der Most RG, et al. Innate immunity defines the capacity of antiviral T cells to limit persistent infection. J Exp Med 2010;207:1333-1343. https://doi.org/10.1084/jem.20091193
  154. Lee SH, Fragoso MF, Biron CA. Cutting edge: a novel mechanism bridging innate and adaptive immunity: IL-12 induction of CD25 to form high-affinity IL-2 receptors on NK cells. J Immunol 2012;189:2712-2716. https://doi.org/10.4049/jimmunol.1201528
  155. Su HC, Nguyen KB, Salazar-Mather TP, Ruzek MC, Dalod MY, Biron CA. NK cell functions restrain T cell responses during viral infections. Eur J Immunol 2001;31:3048-3055. https://doi.org/10.1002/1521-4141(2001010)31:10<3048::AID-IMMU3048>3.0.CO;2-1
  156. Chambers BJ, Salcedo M, Ljunggren HG. Triggering of natural killer cells by the costimulatory molecule CD80 (B7-1). Immunity 1996;5:311-317. https://doi.org/10.1016/S1074-7613(00)80257-5
  157. Carbone E, Terrazzano G, Ruggiero G, Zanzi D, Ottaiano A, Manzo C, Karre K, Zappacosta S. Recognition of autologous dendritic cells by human NK cells. Eur J Immunol 1999;29:4022-4029. https://doi.org/10.1002/(SICI)1521-4141(199912)29:12<4022::AID-IMMU4022>3.0.CO;2-O
  158. Schuster IS, Wikstrom ME, Brizard G, Coudert JD, Estcourt MJ, Manzur M, O'Reilly LA, Smyth MJ, Trapani JA, Hill GR, et al. TRAIL+ NK cells control CD4+ T cell responses during chronic viral infection to limit autoimmunity. Immunity 2014;41:646-656. https://doi.org/10.1016/j.immuni.2014.09.013
  159. Crouse J, Xu HC, Lang PA, Oxenius A. NK cells regulating T cell responses: mechanisms and outcome. Trends Immunol 2015;36:49-58. https://doi.org/10.1016/j.it.2014.11.001
  160. Rabinovich BA, Li J, Shannon J, Hurren R, Chalupny J, Cosman D, Miller RG. Activated, but not resting, T cells can be recognized and killed by syngeneic NK cells. J Immunol 2003;170:3572-3576. https://doi.org/10.4049/jimmunol.170.7.3572
  161. Cerboni C, Zingoni A, Cippitelli M, Piccoli M, Frati L, Santoni A. Antigen-activated human T lymphocytes express cell-surface NKG2D ligands via an ATM/ATR-dependent mechanism and become susceptible to autologous NK- cell lysis. Blood 2007;110:606-615.
  162. Xu HC, Huang J, Pandyra AA, Lang E, Zhuang Y, Thons C, Timm J, Haussinger D, Colonna M, Cantor H, et al. Lymphocytes negatively regulate nk cell activity via Qa-1b following viral infection. Cell Reports 2017;21:2528-2540.
  163. Xu HC, Wang R, Shinde PV, Walotka L, Huang A, Poschmann G, Huang J, Liu W, Stuhler K, Schaal H, et al. Slow viral propagation during initial phase of infection leads to viral persistence in mice. Commun Biol 2021;4:508.