1932

Abstract

Natural killer (NK) cells are innate lymphocytes that provide critical host defense against pathogens and cancer. Originally heralded for their early and rapid effector activity, NK cells have been recognized over the last decade for their ability to undergo adaptive immune processes, including antigen-driven clonal expansion and generation of long-lived memory. This review presents an overview of how NK cells lithely partake in both innate and adaptive responses and how this versatility is manifest in human NK cell–mediated immunity.

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2021-04-26
2024-06-13
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Literature Cited

  1. 1. 
    Spits H, Bernink JH, Lanier L 2016. NK cells and type 1 innate lymphoid cells: partners in host defense. Nat. Immunol. 17:7758–64
    [Google Scholar]
  2. 2. 
    Kondo M, Weissman IL, Akashi K 1997. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 91:5661–72
    [Google Scholar]
  3. 3. 
    Sun JC, Lanier LL. 2011. NK cell development, homeostasis and function: parallels with CD8+ T cells. Nat. Rev. Immunol. 11:10645–57
    [Google Scholar]
  4. 4. 
    Ortaldo JR, Wiltrout RH, Reynolds CW 2014. Natural killer activity: early days, advances, and seminal observations. Crit. Rev. Oncog. 19:121–13
    [Google Scholar]
  5. 5. 
    Herberman RB, Nunn ME, Lavrin DH 1975. Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic and allogeneic tumors: I. Distribution of reactivity and specificity. Int. J. Cancer 16:2216–29
    [Google Scholar]
  6. 6. 
    Kiessling R, Klein E, Wigzell H 1975. “Natural” killer cells in the mouse: I. Cytotoxic cells with specificity for mouse Moloney leukemia cells; specificity and distribution according to genotype. Eur. J. Immunol. 5:2112–17
    [Google Scholar]
  7. 7. 
    Ortaldo JR, Oldham RK, Cannon GC, Herberman RB 1977. Specificity of natural cytotoxic reactivity of normal human lymphocytes against a myeloid leukemia cell line. J. Natl. Cancer Inst. 59:177–82
    [Google Scholar]
  8. 8. 
    Bukowski JF, Woda BA, Habu S, Okumura K, Welsh RM 1983. Natural killer cell depletion enhances virus synthesis and virus-induced hepatitis in vivo. J. Immunol. 131:31531–38
    [Google Scholar]
  9. 9. 
    Sathe P, Delconte RB, Souza-Fonseca-Guimaraes F, Seillet C, Chopin M et al. 2014. Innate immunodeficiency following genetic ablation of Mcl1 in natural killer cells. Nat. Commun. 5:14539
    [Google Scholar]
  10. 10. 
    Mace EM, Orange JS. 2019. Emerging insights into human health and NK cell biology from the study of NK cell deficiencies. Immunol. Rev. 287:1202–25
    [Google Scholar]
  11. 11. 
    Janeway CA. 1989. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol. 54:1–13
    [Google Scholar]
  12. 12. 
    Kiessling R, Petranyi G, Klein G, Wigzell H 1975. Genetic variation of in vitro cytolytic activity and in vivo rejection potential of non‐immunized semi‐syngeneic mice against a mouse lymphoma line. Int. J. Cancer 15:6933–40
    [Google Scholar]
  13. 13. 
    Sendo F, Aoki T, Boyse EA, Buafo CK 1975. Natural occurrence of lymphocytes showing cytotoxic activity to BALB/c radiation-induced leukemia RL male 1 cells. J. Natl. Cancer Inst. 55:3603–9
    [Google Scholar]
  14. 14. 
    Long EO, Kim HS, Liu D, Peterson ME, Rajagopalan S 2013. Controlling natural killer cell responses: integration of signals for activation and inhibition. Annu. Rev. Immunol. 31:227–58
    [Google Scholar]
  15. 15. 
    Kärre 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]
  16. 16. 
    Ljunggren H-G, Kärre K. 1990. In search of the “missing self”: MHC molecules and NK cell recognition. Immunol. Today 11:7237–44
    [Google Scholar]
  17. 17. 
    Barry KC, Hsu J, Broz ML, Cueto FJ, Binnewies M et al. 2018. A natural killer-dendritic cell axis defines checkpoint therapy-responsive tumor microenvironments. Nat. Med. 24:81178–91
    [Google Scholar]
  18. 18. 
    Böttcher JP, Bonavita E, Chakravarty P, Blees H, Cabeza-Cabrerizo M et al. 2018. NK cells stimulate recruitment of cDC1 into the tumor microenvironment promoting cancer immune control. Cell 172:51022–37.e14
    [Google Scholar]
  19. 19. 
    Burnet FM. 1976. A modification of Jerne's theory of antibody production using the concept of clonal selection. CA Cancer J. Clin. 26:2119–21
    [Google Scholar]
  20. 20. 
    Smith KA. 2012. Toward a molecular understanding of adaptive immunity: a chronology, part I. Front. Immunol. 3:369
    [Google Scholar]
  21. 21. 
    Schatz DG, Ji Y. 2011. Recombination centres and the orchestration of V(D)J recombination. Nat. Rev. Immunol. 11:4251–63
    [Google Scholar]
  22. 22. 
    Casrouge A, Beaudoing E, Dalle S, Pannetier C, Kanellopoulos J, Kourilsky P 2000. Size estimate of the αβ TCR repertoire of naive mouse splenocytes. J. Immunol. 164:115782–87
    [Google Scholar]
  23. 23. 
    Arstila TP, Casrouge A, Baron V, Even J, Kanellopoulos J, Kourilsky P 1999. A direct estimate of the human αβ T cell receptor diversity. Science 286:5441958–61
    [Google Scholar]
  24. 24. 
    Badovinac VP, Haring JS, Harty JT 2007. Initial T cell receptor transgenic cell precursor frequency dictates critical aspects of the CD8+ T cell response to infection. Immunity 26:6827–41
    [Google Scholar]
  25. 25. 
    Kaech SM, Cui W. 2012. Transcriptional control of effector and memory CD8+ T cell differentiation. Nat. Rev. Immunol. 12:11749–61
    [Google Scholar]
  26. 26. 
    Sun JC, Beilke JN, Lanier LL 2009. Adaptive immune features of natural killer cells. Nature 457:7229557–61
    [Google Scholar]
  27. 27. 
    Santo JPD, Muller W, Guy-Grand D, Fischer A, Rajewsky K 1995. Lymphoid development in mice with a targeted deletion of the interleukin 2 receptor gamma chain. PNAS 92:2377–81
    [Google Scholar]
  28. 28. 
    Vosshenrich CAJ, Ranson T, Samson SI, Corcuff E, Colucci F et al. 2005. Roles for common cytokine receptor γ-chain-dependent cytokines in the generation, differentiation, and maturation of NK cell precursors and peripheral NK cells in vivo. J. Immunol. 174:31213–21
    [Google Scholar]
  29. 29. 
    Kee BL, Morman RE, Sun M 2020. Transcriptional regulation of natural killer cell development and maturation. Adv. Immunol. 146:1–28
    [Google Scholar]
  30. 30. 
    Lanier LL. 1998. NK cell receptors. Annu. Rev. Immunol. 16:359–93
    [Google Scholar]
  31. 31. 
    Horowitz A, Strauss-Albee DM, Leipold M, Kubo J, Nemat-Gorgani N et al. 2013. Genetic and environmental determinants of human NK cell diversity revealed by mass cytometry. Sci. Transl. Med. 5:208208ra145
    [Google Scholar]
  32. 32. 
    Orr MT, Lanier LL. 2010. Natural killer cell education and tolerance. Cell 142:6847–56
    [Google Scholar]
  33. 33. 
    Chiossone L, Chaix J, Fuseri N, Roth C, Vivier E, Walzer T 2009. Maturation of mouse NK cells is a 4-stage developmental program. Blood 113:225488–96
    [Google Scholar]
  34. 34. 
    Kim S, Iizuka K, Kang H-SP, Dokun A, French AR et al. 2002. In vivo developmental stages in murine natural killer cell maturation. Nat. Immunol. 3:6523–28
    [Google Scholar]
  35. 35. 
    Hayakawa Y, Smyth MJ. 2006. CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J. Immunol. 176:31517–24
    [Google Scholar]
  36. 36. 
    Kamimura Y, Lanier LL. 2015. Homeostatic control of memory cell progenitors in the natural killer cell lineage. Cell Rep. 10:2280–91
    [Google Scholar]
  37. 37. 
    Delconte RB, Guittard G, Goh W, Hediyeh-Zadeh S, Hennessy RJ et al. 2020. NK cell priming from endogenous homeostatic signals is modulated by CIS. Front. Immunol. 11:75
    [Google Scholar]
  38. 38. 
    Guan J, Miah SMS, Wilson ZS, Erick TK, Banh C, Brossay L 2014. Role of type I interferon receptor signaling on NK cell development and functions. PLOS ONE 9:10e111302
    [Google Scholar]
  39. 39. 
    Klose CSN, Artis D. 2016. Innate lymphoid cells as regulators of immunity, inflammation and tissue homeostasis. Nat. Immunol. 17:7765–74
    [Google Scholar]
  40. 40. 
    Weizman O-E, Adams NM, Schuster IS, Krishna C, Pritykin Y et al. 2017. ILC1 confer early host protection at initial sites of viral infection. Cell 171:4795–808.e12
    [Google Scholar]
  41. 41. 
    Angelo LS, Banerjee PP, Monaco-Shawver L, Rosen JB, Makedonas G et al. 2015. Practical NK cell phenotyping and variability in healthy adults. Immunol. Res. 62:3341–56
    [Google Scholar]
  42. 42. 
    Michel T, Poli A, Cuapio A, Briquemont B, Iserentant G et al. 2016. Human CD56bright NK cells: an update. J. Immunol. 196:72923–31
    [Google Scholar]
  43. 43. 
    Chan A, Hong D-L, Atzberger A, Kollnberger S, Filer AD et al. 2007. CD56bright human NK cells differentiate into CD56dim cells: role of contact with peripheral fibroblasts. J. Immunol. 179:189–94
    [Google Scholar]
  44. 44. 
    Romagnani C, Juelke K, Falco M, Morandi B, D'Agostino A et al. 2007. CD56brightCD16 killer Ig-like receptor NK cells display longer telomeres and acquire features of CD56dim NK cells upon activation. J. Immunol. 178:84947–55
    [Google Scholar]
  45. 45. 
    Crinier A, Milpied P, Escalière 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 49:5971–86.e5
    [Google Scholar]
  46. 46. 
    Wu C, Li B, Lu R, Koelle SJ, Yang Y et al. 2014. Clonal tracking of rhesus macaque hematopoiesis highlights a distinct lineage origin for natural killer cells. Cell Stem Cell 14:4486–99
    [Google Scholar]
  47. 47. 
    Marquardt N, Béziat V, Nyström S, Hengst J, Ivarsson MA et al. 2015. Cutting edge: identification and characterization of human intrahepatic CD49a+ NK cells. J. Immunol. 194:62467–71
    [Google Scholar]
  48. 48. 
    Scoville SD, Mundy-Bosse BL, Zhang MH, Chen L, Zhang X et al. 2016. A progenitor cell expressing transcription factor RORγt generates all human innate lymphoid cell subsets. Immunity 44:51140–50
    [Google Scholar]
  49. 49. 
    Fehniger TA, Cai SF, Cao X, Bredemeyer AJ, Presti RM et al. 2007. Acquisition of murine NK cell cytotoxicity requires the translation of a pre-existing pool of granzyme B and perforin mRNAs. Immunity 26:6798–811
    [Google Scholar]
  50. 50. 
    Bezman NA, Kim CC, Sun JC, Min-Oo G, Hendricks DW et al. 2012. Molecular definition of the identity and activation of natural killer cells. Nat. Immunol. 13:101000–9
    [Google Scholar]
  51. 51. 
    Reinhardt RL, Liang H-E, Bao K, Price AE, Mohrs M et al. 2015. A novel model for IFN-γ-mediated autoinflammatory syndromes. J. Immunol. 194:52358–68
    [Google Scholar]
  52. 52. 
    Lau CM, Adams NM, Geary CD, Weizman O-E, Rapp M et al. 2018. Epigenetic control of innate and adaptive immune memory. Nat. Immunol. 19:9963–72
    [Google Scholar]
  53. 53. 
    Zook EC, Li Z-Y, Xu Y, de Pooter RF, Verykokakis M et al. 2018. Transcription factor ID2 prevents E proteins from enforcing a naïve T lymphocyte gene program during NK cell development. Sci. Immunol. 3:22eaao2139
    [Google Scholar]
  54. 54. 
    Marçais A, Cherfils-Vicini J, Viant C, Degouve S, Viel S et al. 2014. The metabolic checkpoint kinase mTOR is essential for IL-15 signaling during the development and activation of NK cells. Nat. Immunol. 15:8749–57
    [Google Scholar]
  55. 55. 
    Keppel MP, Saucier N, Mah AY, Vogel TP, Cooper MA 2015. Activation-specific metabolic requirements for NK cell IFN-γ production. J. Immunol. 194:41954–62
    [Google Scholar]
  56. 56. 
    Takeda K, Tsutsui H, Yoshimoto T, Adachi O, Yoshida N et al. 1998. Defective NK cell activity and Th1 response in IL-18-deficient mice. Immunity 8:3383–90
    [Google Scholar]
  57. 57. 
    Chaix J, Tessmer MS, Hoebe K, Fuséri N, Ryffel B et al. 2008. Priming of NK cells by IL-18. J. Immunol. 181:31627–31
    [Google Scholar]
  58. 58. 
    Kim S, Poursine-Laurent J, Truscott SM, Lybarger L, Song Y-J et al. 2005. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 436:7051709–13
    [Google Scholar]
  59. 59. 
    Joncker NT, Fernandez NC, Treiner E, Vivier E, Raulet DH 2009. NK cell responsiveness is tuned commensurate with the number of inhibitory receptors for self-MHC class I: the rheostat model. J. Immunol. 182:84572–80
    [Google Scholar]
  60. 60. 
    Boudreau JE, Hsu KC. 2018. Natural killer cell education and the response to infection and cancer therapy: Stay tuned. Trends Immunol. 39:3222–39
    [Google Scholar]
  61. 61. 
    Virgin HW, Wherry EJ, Ahmed R 2009. Redefining chronic viral infection. Cell 138:130–50
    [Google Scholar]
  62. 62. 
    Biron CA, Byron KS, Sullivan JL 1989. Severe herpesvirus infections in an adolescent without natural killer cells. N. Engl. J. Med. 320:261731–35
    [Google Scholar]
  63. 63. 
    Orange JS. 2013. Natural killer cell deficiency. J. Allergy Clin. Immun. 132:3515–25
    [Google Scholar]
  64. 64. 
    Manicklal S, Emery VC, Lazzarotto T, Boppana SB, Gupta RK 2013. The “silent” global burden of congenital cytomegalovirus. Clin. Microbiol. Rev. 26:186–102
    [Google Scholar]
  65. 65. 
    Styczynski J. 2018. Who is the patient at risk of CMV recurrence: a review of the current scientific evidence with a focus on hematopoietic cell transplantation. Infect. Dis. Ther. 7:11–16
    [Google Scholar]
  66. 66. 
    Habu S, Akamatsu K, Tamaoki N, Okumura K 1984. In vivo significance of NK cell on resistance against virus (HSV-1) infections in mice. J. Immunol. 133:52743–47
    [Google Scholar]
  67. 67. 
    Parker AK, Parker S, Yokoyama WM, Corbett JA, Buller RML 2007. Induction of natural killer cell responses by ectromelia virus controls infection. J. Virol. 81:84070–79
    [Google Scholar]
  68. 68. 
    Tabeta K, Georgel P, Janssen E, Du X, Hoebe K et al. 2004. Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. PNAS 101:103516–21
    [Google Scholar]
  69. 69. 
    Krug A, French AR, Barchet W, Fischer JAA, Dzionek A et al. 2004. TLR9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function. Immunity 21:1107–19
    [Google Scholar]
  70. 70. 
    Lio C-WJ, McDonald B, Takahashi M, Dhanwani R, Sharma N et al. 2016. cGAS-STING signaling regulates initial innate control of cytomegalovirus infection. J. Virol. 90:177789–97
    [Google Scholar]
  71. 71. 
    Swiecki M, Gilfillan S, Vermi W, Wang Y, Colonna M 2010. Plasmacytoid dendritic cell ablation impacts early interferon responses and antiviral NK and CD8+ T cell accrual. Immunity 33:6955–66
    [Google Scholar]
  72. 72. 
    Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP 1999. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu. Rev. Immunol. 17:189–220
    [Google Scholar]
  73. 73. 
    Degli-Esposti MA, Smyth MJ. 2005. Close encounters of different kinds: dendritic cells and NK cells take centre stage. Nat. Rev. Immunol. 5:2112–24
    [Google Scholar]
  74. 74. 
    McGeoch DJ, Cook S, Dolan A, Jamieson FE, Telford EAR 1995. Molecular phylogeny and evolutionary timescale for the family of mammalian herpesviruses. J. Mol. Biol. 247:3443–58
    [Google Scholar]
  75. 75. 
    Rawlinson WD, Farrell HE, Barrell BG 1996. Analysis of the complete DNA sequence of murine cytomegalovirus. J. Virol. 70:128833–49
    [Google Scholar]
  76. 76. 
    Staczek J. 1990. Animal cytomegaloviruses. Microbiol. Rev. 54:3247–65
    [Google Scholar]
  77. 77. 
    Farrell HE, Davis-Poynter NJ, Andrews DM, Degli-Esposti MA 2002. Function of CMV-encoded MHC class I homologues. Curr. Top. Microbiol. 269:131–51
    [Google Scholar]
  78. 78. 
    Scalzo AA, Fitzgerald NA, Simmons A, Vista ABL, Shellam GR 1990. Cmv-1, a genetic locus that controls murine cytomegalovirus replication in the spleen. J. Exp. Med. 171:51469–83
    [Google Scholar]
  79. 79. 
    Scalzo AA, Lyons PA, Fitzgerald NA, Forbes CA, Yokoyama WM, Shellam GR 1995. Genetic mapping of Cmv1 in the region of mouse chromosome 6 encoding the NK gene complex-associated loci Ly49 and musNKR-P1. Genomics 27:3435–41
    [Google Scholar]
  80. 80. 
    Lee S-H, Girard S, Macina D, Busà 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. 28:142–45
    [Google Scholar]
  81. 81. 
    Brown MG, Dokun AO, Heusel JW, Smith HRC, Beckman DL et al. 2001. Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science 292:5518934–37
    [Google Scholar]
  82. 82. 
    Smith KM, Wu J, Bakker ABH, Phillips JH, Lanier LL 1998. Ly-49D and Ly-49H associate with mouse DAP12 and form activating receptors. J. Immunol. 161:17–10
    [Google Scholar]
  83. 83. 
    Lanier LL. 2008. Up on the tightrope: natural killer cell activation and inhibition. Nat. Immunol. 9:5495–502
    [Google Scholar]
  84. 84. 
    Fodil-Cornu N, Lee S-H, Belanger S, Makrigiannis AP, Biron CA et al. 2008. Ly49h-deficient C57BL/6 mice: A new mouse cytomegalovirus-susceptible model remains resistant to unrelated pathogens controlled by the NK gene complex. J. Immunol. 181:96394–405
    [Google Scholar]
  85. 85. 
    Sjölin H, Tomasello E, Mousavi-Jazi M, Bartolazzi A, Kärre K et al. 2002. Pivotal role of KARAP/DAP12 adaptor molecule in the natural killer cell-mediated resistance to murine cytomegalovirus infection. J. Exp. Med. 195:7825–34
    [Google Scholar]
  86. 86. 
    Daniels KA, Devora G, Lai WC, O'Donnell CL, Bennett M, Welsh RM 2001. Murine cytomegalovirus is regulated by a discrete subset of natural killer cells reactive with monoclonal antibody to Ly49h. J. Exp. Med. 194:129–44
    [Google Scholar]
  87. 87. 
    Lee S-H, Zafer A, de Repentigny Y, Kothary R, Tremblay ML et al. 2003. Transgenic expression of the activating natural killer receptor Ly49H confers resistance to cytomegalovirus in genetically susceptible mice. J. Exp. Med. 197:4515–26
    [Google Scholar]
  88. 88. 
    Arase H, Mocarski ES, Campbell AE, Hill AB, Lanier LL 2002. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296:55711323–26
    [Google Scholar]
  89. 89. 
    Smith HRC, 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 99:138826–31
    [Google Scholar]
  90. 90. 
    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 104:2410128–33
    [Google Scholar]
  91. 91. 
    Rodriguez M, Sabastian P, Clark P, Brown MG 2004. Cmv1-independent antiviral role of NK cells revealed in murine cytomegalovirus-infected New Zealand white mice. J. Immunol. 173:106312–18
    [Google Scholar]
  92. 92. 
    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. 186:31713–22
    [Google Scholar]
  93. 93. 
    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 20:6747–56
    [Google Scholar]
  94. 94. 
    Dokun AO, Kim S, Smith HRC, Kang H-SP, Chu DT, Yokoyama WM 2001. Specific and nonspecific NK cell activation during virus infection. Nat. Immunol. 2:10951–56
    [Google Scholar]
  95. 95. 
    Nabekura T, Lanier LL. 2016. Tracking the fate of antigen-specific versus cytokine-activated natural killer cells after cytomegalovirus infection. J. Exp. Med. 213:122745–58
    [Google Scholar]
  96. 96. 
    Weng N, Araki Y, Subedi K 2012. The molecular basis of the memory T cell response: differential gene expression and its epigenetic regulation. Nat. Rev. Immunol. 12:4306–15
    [Google Scholar]
  97. 97. 
    Adams NM, Geary CD, Santosa EK, Lumaquin D, Luduec J-BL et al. 2019. Cytomegalovirus infection drives avidity selection of natural killer cells. Immunity 50:61381–90.e5
    [Google Scholar]
  98. 98. 
    Min-Oo G, Lanier LL. 2014. Cytomegalovirus generates long-lived antigen-specific NK cells with diminished bystander activation to heterologous infection. J. Exp. Med. 211:132669–80
    [Google Scholar]
  99. 99. 
    Berg RE, Crossley E, Murray S, Forman J 2003. Memory CD8+ T cells provide innate immune protection against Listeriamonocytogenes in the absence of cognate antigen. J. Exp. Med. 198:101583–93
    [Google Scholar]
  100. 100. 
    Chu T, Tyznik AJ, Roepke S, Berkley AM, Woodward-Davis A et al. 2013. Bystander-activated memory CD8 T cells control early pathogen load in an innate-like, NKG2D-dependent manner. Cell Rep. 3:3701–8
    [Google Scholar]
  101. 101. 
    Chalmer JE, Mackenzie JS, Stanley NF 1977. Resistance to murine cytomegalovirus linked to the major histocompatibility complex of the mouse. J. Gen. Virol. 37:1107–14
    [Google Scholar]
  102. 102. 
    Desrosiers M-P, Kielczewska A, Loredo-Osti J-C, 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. 37:6593–99
    [Google Scholar]
  103. 103. 
    Kleijnen MF, Huppa JB, Lucin P, Mukherjee S, Farrell H 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. 16:4685–94
    [Google Scholar]
  104. 104. 
    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. 216:81809–27
    [Google Scholar]
  105. 105. 
    Pyzik M, Charbonneau B, Gendron-Pontbriand E-M, Babić M, Krmpotić A et al. 2011. Distinct MHC class I-dependent NK cell-activating receptors control cytomegalovirus infection in different mouse strains. J. Exp. Med. 208:51105–17
    [Google Scholar]
  106. 106. 
    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. 206:3515–23
    [Google Scholar]
  107. 107. 
    Lanier LL. 2001. On guard—activating NK cell receptors. Nat. Immunol. 2:123–27
    [Google Scholar]
  108. 108. 
    Aguilar OA, Berry R, Rahim MMA, Reichel JJ, Popović B et al. 2017. A viral immunoevasin controls innate immunity by targeting the prototypical natural killer cell receptor family. Cell 169:158–71.e14
    [Google Scholar]
  109. 109. 
    Weizman O-E, 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. 20:81004–11
    [Google Scholar]
  110. 110. 
    Nabekura T, Lanier LL. 2014. Antigen-specific expansion and differentiation of natural killer cells by alloantigen stimulation. J. Exp. Med. 211:122455–65
    [Google Scholar]
  111. 111. 
    Gumá M, Angulo A, Vilches C, Gómez-Lozano N, Malats N, López-Botet M 2004. Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood 104:123664–71
    [Google Scholar]
  112. 112. 
    Braud VM, Allan DSJ, O'Callaghan CA, Söderström K, D'Andrea A et al. 1998. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391:6669795–99
    [Google Scholar]
  113. 113. 
    Lanier LL, Corliss B, Wu J, Phillips JH 1998. Association of DAP12 with activating CD94/NKG2C NK cell receptors. Immunity 8:6693–701
    [Google Scholar]
  114. 114. 
    Lopez-Vergès S, Milush JM, Schwartz BS, Pando MJ, Jarjoura J et al. 2011. Expansion of a unique CD57+NKG2Chi natural killer cell subset during acute human cytomegalovirus infection. PNAS 108:3614725–32
    [Google Scholar]
  115. 115. 
    Chiesa MD, Falco M, Podestà M, Locatelli F, Moretta L et al. 2012. Phenotypic and functional heterogeneity of human NK cells developing after umbilical cord blood transplantation: a role for human cytomegalovirus. ? Blood 119:2399–410
    [Google Scholar]
  116. 116. 
    Foley B, Cooley S, Verneris MR, Curtsinger J, Luo X et al. 2012. Human cytomegalovirus (CMV)-induced memory-like NKG2C+ NK cells are transplantable and expand in vivo in response to recipient CMV antigen. J. Immunol. 189:105082–88
    [Google Scholar]
  117. 117. 
    Kuijpers TW, Baars PA, Dantin C, van den Burg M, van Lier RAW, Roosnek E 2008. Human NK cells can control CMV infection in the absence of T cells. Blood 112:3914–15
    [Google Scholar]
  118. 118. 
    Björkström NK, Lindgren T, Stoltz M, Fauriat C, Braun M et al. 2011. Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus. J. Exp. Med. 208:113–21
    [Google Scholar]
  119. 119. 
    Petitdemange C, Becquart P, Wauquier N, Béziat V, Debré P et al. 2011. Unconventional repertoire profile is imprinted during acute chikungunya infection for natural killer cells polarization toward cytotoxicity. PLOS Pathog. 7:9e1002268
    [Google Scholar]
  120. 120. 
    Gumá M, Cabrera C, Erkizia I, Bofill M, Clotet B 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. 194:138–41
    [Google Scholar]
  121. 121. 
    Hendricks DW, Balfour HH, Dunmire SK, Schmeling DO, Hogquist KA, Lanier LL 2014. NKG2ChiCD57+ NK cells respond specifically to acute infection with cytomegalovirus and not Epstein-Barr virus. J. Immunol. 192:104492–96
    [Google Scholar]
  122. 122. 
    Björkström NK, Svensson A, Malmberg K-J, Eriksson K, Ljunggren H-G 2011. Characterization of natural killer cell phenotype and function during recurrent human HSV-2 infection. PLOS ONE 6:11e27664
    [Google Scholar]
  123. 123. 
    Michaëlsson J, de Matos CT, Achour A, Lanier LL, Kärre K, Söderström K 2002. A signal peptide derived from hsp60 binds HLA-E and interferes with CD94/NKG2A recognition. J. Exp. Med. 196:111403–14
    [Google Scholar]
  124. 124. 
    Ulbrecht M, Martinozzi S, Grzeschik M, Hengel H, Ellwart JW 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. 164:105019–22
    [Google Scholar]
  125. 125. 
    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 287:54551031–33
    [Google Scholar]
  126. 126. 
    Rölle A, Pollmann J, Ewen E-M, Le VTK, Halenius A et al. 2014. IL-12-producing monocytes and HLA-E control HCMV-driven NKG2C+ NK cell expansion. J. Clin. Investig. 124:125305–16
    [Google Scholar]
  127. 127. 
    Gumá M, Budt M, Sáez A, Brckalo T, Hengel H et al. 2006. Expansion of CD94/NKG2C+ NK cells in response to human cytomegalovirus-infected fibroblasts. Blood. 107:93624–31
    [Google Scholar]
  128. 128. 
    Hammer Q, Rückert T, Borst EM, Dunst J, Haubner A et al. 2018. Peptide-specific recognition of human cytomegalovirus strains controls adaptive natural killer cells. Nat. Immunol. 19:5453–63
    [Google Scholar]
  129. 129. 
    Béziat V, Liu LL, Malmberg J-A, Ivarsson MA, Sohlberg E et al. 2013. NK cell responses to cytomegalovirus infection lead to stable imprints in the human KIR repertoire and involve activating KIRs. Blood 121:142678–88
    [Google Scholar]
  130. 130. 
    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 42:3443–56
    [Google Scholar]
  131. 131. 
    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 42:3431–42
    [Google Scholar]
  132. 132. 
    Luetke-Eversloh M, Hammer Q, Durek P, Nordström K, Gasparoni G et al. 2014. Human cytomegalovirus drives epigenetic imprinting of the IFNG locus in NKG2Chi natural killer cells. PLOS Pathog. 10:10e1004441
    [Google Scholar]
  133. 133. 
    Wu Z, Sinzger C, Frascaroli G, Reichel J, Bayer C et al. 2013. Human cytomegalovirus-induced NKG2Chi CD57hi natural killer cells are effectors dependent on humoral antiviral immunity. J. Virol. 87:137717–25
    [Google Scholar]
  134. 134. 
    Peppa D, Pedroza-Pacheco I, Pellegrino P, Williams I, Maini MK, Borrow P 2018. Adaptive reconfiguration of natural killer cells in HIV-1 infection. Front. Immunol. 9:474
    [Google Scholar]
  135. 135. 
    Azzi T, Lünemann A, Murer A, Ueda S, Béziat V et al. 2014. Role for early-differentiated natural killer cells in infectious mononucleosis. Blood 124:162533–43
    [Google Scholar]
  136. 136. 
    Wijaya RS, Read SA, Truong NR, Han S, Chen D et al. 2021. HBV vaccination and HBV infection induces HBV-specific natural killer cell memory. Gut 70:2357–69
    [Google Scholar]
  137. 137. 
    Nabekura T, Lanier LL. 2016. Activating receptors for self-MHC class I enhance effector functions and memory differentiation of NK cells during mouse cytomegalovirus infection. Immunity 45:174–82
    [Google Scholar]
  138. 138. 
    Davis AH, Guseva NV, Ball BL, Heusel JW 2008. Characterization of murine cytomegalovirus m157 from infected cells and identification of critical residues mediating recognition by the NK cell receptor Ly49H. J. Immunol. 181:1265–75
    [Google Scholar]
  139. 139. 
    Guseva NV, Fullenkamp CA, Naumann PW, Shey MR, Ballas ZK et al. 2010. Glycosylation contributes to variability in expression of murine cytomegalovirus m157 and enhances stability of interaction with the NK‐cell receptor Ly49H. Eur. J. Immunol. 40:92618–31
    [Google Scholar]
  140. 140. 
    Heatley SL, Pietra G, Lin J, Widjaja JML, 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. 288:128679–90
    [Google Scholar]
  141. 141. 
    Rölle A, Meyer M, Calderazzo S, Jäger D, Momburg F 2018. Distinct HLA-E peptide complexes modify antibody-driven effector functions of adaptive NK cells. Cell Rep. 24:81967–76.e4
    [Google Scholar]
  142. 142. 
    Orr MT, Sun JC, Hesslein DGT, Arase H, Phillips JH et al. 2009. Ly49H signaling through DAP10 is essential for optimal natural killer cell responses to mouse cytomegalovirus infection. J. Exp. Med. 206:4807–17
    [Google Scholar]
  143. 143. 
    Nabekura T, Gotthardt D, Niizuma K, Trsan T, Jenus T et al. 2017. NKG2D signaling enhances NK cell responses but alone is insufficient to drive expansion during mouse cytomegalovirus infection. J. Immunol. 199:51567–71
    [Google Scholar]
  144. 144. 
    Nabekura T, Kanaya M, Shibuya A, Fu G, Gascoigne NRJ, Lanier LL 2014. Costimulatory molecule DNAM-1 is essential for optimal differentiation of memory natural killer cells during mouse cytomegalovirus infection. Immunity 40:2225–34
    [Google Scholar]
  145. 145. 
    Liu LL, Landskron J, Ask EH, Enqvist M, Sohlberg E et al. 2016. Critical role of CD2 co-stimulation in adaptive natural killer cell responses revealed in NKG2C-deficient humans. Cell Rep. 15:51088–99
    [Google Scholar]
  146. 146. 
    Rölle A, Halenius A, Ewen E, Cerwenka A, Hengel H, Momburg F 2016. CD2-CD58 interactions are pivotal for the activation and function of adaptive natural killer cells in human cytomegalovirus infection. Eur. J. Immunol. 46:102420–25
    [Google Scholar]
  147. 147. 
    Berry R, Watson GM, Jonjic S, Degli-Esposti MA, Rossjohn J 2020. Modulation of innate and adaptive immunity by cytomegaloviruses. Nat. Rev. Immunol. 20:2113–27
    [Google Scholar]
  148. 148. 
    Orr MT, Murphy WJ, Lanier LL 2010. “Unlicensed” natural killer cells dominate the response to cytomegalovirus infection. Nat. Immunol. 11:4321–27
    [Google Scholar]
  149. 149. 
    Stojanovic A, Fiegler N, Brunner-Weinzierl M, Cerwenka A 2014. CTLA-4 is expressed by activated mouse NK cells and inhibits NK cell IFN-γ production in response to mature dendritic cells. J. Immunol. 192:94184–91
    [Google Scholar]
  150. 150. 
    Hsu J, Hodgins JJ, Marathe M, Nicolai CJ, Bourgeois-Daigneault M-C et al. 2018. Contribution of NK cells to immunotherapy mediated by PD-1/PD-L1 blockade. J. Clin. Investig. 128:104654–68
    [Google Scholar]
  151. 151. 
    Zhang Q, Bi J, Zheng X, Chen Y, Wang H et al. 2018. Blockade of the checkpoint receptor TIGIT prevents NK cell exhaustion and elicits potent anti-tumor immunity. Nat. Immunol. 19:7723–32
    [Google Scholar]
  152. 152. 
    Quatrini L, Wieduwild E, Escaliere B, Filtjens J, Chasson L et al. 2018. Endogenous glucocorticoids control host resistance to viral infection through the tissue-specific regulation of PD-1 expression on NK cells. Nat. Immunol. 19:9954–62
    [Google Scholar]
  153. 153. 
    Aguilar OA, Sampaio IS, Rahim MMA, Samaniego JD, Tilahun ME et al. 2019. Mouse cytomegalovirus m153 protein stabilizes expression of the inhibitory NKR-P1B ligand Clr-b. J. Virol. 94:1e01220–19
    [Google Scholar]
  154. 154. 
    Sun JC, Madera S, Bezman NA, Beilke JN, Kaplan MH, Lanier LL 2012. Proinflammatory cytokine signaling required for the generation of natural killer cell memory. J. Exp. Med. 209:5947–54
    [Google Scholar]
  155. 155. 
    Beaulieu AM, Zawislak CL, Nakayama T, Sun JC 2014. The transcription factor Zbtb32 controls the proliferative burst of virus-specific natural killer cells responding to infection. Nat. Immunol. 15:6ni.2876
    [Google Scholar]
  156. 156. 
    Adams NM, Lau CM, Fan X, Rapp M, Geary CD et al. 2018. Transcription factor IRF8 orchestrates the adaptive natural killer cell response. Immunity 48:61172–82.e6
    [Google Scholar]
  157. 157. 
    Madera S, Geary CD, Lau CM, Pikovskaya O, Reiner SL, Sun JC 2018. Divergent requirement of T-box transcription factors in effector and memory NK cells. J. Immunol. 200:61977–81
    [Google Scholar]
  158. 158. 
    Rapp M, Lau CM, Adams NM, Weizman O-E, O'Sullivan TE et al. 2017. Core-binding factor β and Runx transcription factors promote adaptive natural killer cell responses. Sci. Immunol. 2:18eaan3796
    [Google Scholar]
  159. 159. 
    Diaz-Salazar C, Bou-Puerto R, Mujal AM, Lau CM, von Hoesslin M et al. 2020. Cell-intrinsic adrenergic signaling controls the adaptive NK cell response to viral infection. J. Exp. Med. 217:4e20190549
    [Google Scholar]
  160. 160. 
    Lee S-H, Fragoso MF, Biron CA 2012. 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. 189:62712–16
    [Google Scholar]
  161. 161. 
    Ross SH, Cantrell DA. 2018. Signaling and function of interleukin-2 in T lymphocytes. Annu. Rev. Immunol. 36:411–33
    [Google Scholar]
  162. 162. 
    Sun JC, Ma A, Lanier LL 2009. IL-15-independent NK cell response to mouse cytomegalovirus infection. J. Immunol. 183:52911–14
    [Google Scholar]
  163. 163. 
    Ohs I, van den Broek M, Nussbaum K, Münz C, Arnold SJ et al. 2016. Interleukin-12 bypasses common gamma-chain signalling in emergency natural killer cell lymphopoiesis. Nat. Commun. 7:113708
    [Google Scholar]
  164. 164. 
    Madera S, Sun JC. 2015. Stage-specific requirement of IL-18 for antiviral NK cell expansion. J. Immunol. 194:41408–12
    [Google Scholar]
  165. 165. 
    Andrews DM, Scalzo AA, Yokoyama WM, Smyth MJ, Degli-Esposti MA 2003. Functional interactions between dendritic cells and NK cells during viral infection. Nat. Immunol. 4:2175–81
    [Google Scholar]
  166. 166. 
    Nabekura T, Girard J-P, Lanier LL 2015. IL-33 receptor ST2 amplifies the expansion of NK cells and enhances host defense during mouse cytomegalovirus infection. J. Immunol. 194:125948–52
    [Google Scholar]
  167. 167. 
    Zawislak CL, Beaulieu AM, Loeb GB, Karo J, Canner D et al. 2013. Stage-specific regulation of natural killer cell homeostasis and response against viral infection by microRNA-155. PNAS 110:176967–72
    [Google Scholar]
  168. 168. 
    Madera S, Rapp M, Firth MA, Beilke JN, Lanier LL, Sun JC 2016. Type I IFN promotes NK cell expansion during viral infection by protecting NK cells against fratricide. J. Exp. Med. 213:2225–33
    [Google Scholar]
  169. 169. 
    Geary CD, Krishna C, Lau CM, Adams NM, Gearty SV et al. 2018. Non-redundant ISGF3 components promote NK cell survival in an auto-regulatory manner during viral infection. Cell Rep. 24:81949–57.e6
    [Google Scholar]
  170. 170. 
    Lam VC, Folkersen L, Aguilar OA, Lanier LL 2019. KLF12 regulates mouse NK cell proliferation. J. Immunol. 203:4981–89
    [Google Scholar]
  171. 171. 
    Kasaian MT, Whitters MJ, Carter LL, Lowe LD, Jussif JM et al. 2002. IL-21 limits NK cell responses and promotes antigen-specific T cell activation: a mediator of the transition from innate to adaptive immunity. Immunity 16:4559–69
    [Google Scholar]
  172. 172. 
    Parrish-Novak J, Dillon SR, Nelson A, Hammond A, Sprecher C et al. 2000. Interleukin 21 and its receptor are involved in NK cell expansion and regulation of lymphocyte function. Nature 408:680857–63
    [Google Scholar]
  173. 173. 
    Cortez VS, Ulland TK, Cervantes-Barragan L, Bando JK, Robinette ML et al. 2017. SMAD4 impedes the conversion of NK cells into ILC1-like cells by curtailing non-canonical TGF-β signaling. Nat. Immunol. 18:9995–1003
    [Google Scholar]
  174. 174. 
    Gao Y, Souza-Fonseca-Guimaraes F, Bald T, Ng SS, Young A et al. 2017. Tumor immunoevasion by the conversion of effector NK cells into type 1 innate lymphoid cells. Nat. Immunol. 18:91004–15
    [Google Scholar]
  175. 175. 
    Loftus RM, Assmann N, Kedia-Mehta N, O'Brien KL, Garcia A et al. 2018. Amino acid-dependent cMyc expression is essential for NK cell metabolic and functional responses in mice. Nat. Commun. 9:12341
    [Google Scholar]
  176. 176. 
    Dong H, Adams NM, Xu Y, Cao J, Allan DSJ et al. 2019. The IRE1 endoplasmic reticulum stress sensor activates natural killer cell immunity in part by regulating c-Myc. Nat. Immunol. 20:7865–78
    [Google Scholar]
  177. 177. 
    Donnelly RP, Loftus RM, Keating SE, Liou KT, Biron CA et al. 2014. mTORC1-dependent metabolic reprogramming is a prerequisite for NK cell effector function. J. Immunol. 193:94477–84
    [Google Scholar]
  178. 178. 
    Assmann N, O'Brien KL, Donnelly RP, Dyck L, Zaiatz-Bittencourt V et al. 2017. Srebp-controlled glucose metabolism is essential for NK cell functional responses. Nat. Immunol. 18:111197–206
    [Google Scholar]
  179. 179. 
    Mah AY, Rashidi A, Keppel MP, Saucier N, Moore EK et al. 2017. Glycolytic requirement for NK cell cytotoxicity and cytomegalovirus control. JCI Insight 2:23e95128
    [Google Scholar]
  180. 180. 
    Nandagopal N, Ali AK, Komal AK, Lee S-H 2014. The critical role of IL-15-PI3K-mTOR pathway in natural killer cell effector functions. Front. Immunol. 5:187
    [Google Scholar]
  181. 181. 
    O'Sullivan TE, Johnson LR, Kang HH, Sun JC 2015. BNIP3- and BNIP3L-mediated mitophagy promotes the generation of natural killer cell memory. Immunity 43:2331–42
    [Google Scholar]
  182. 182. 
    Cichocki F, Wu C-Y, Zhang B, Felices M, Tesi B et al. 2018. ARID5B regulates metabolic programming in human adaptive NK cells. J. Exp. Med. 215:92379–95
    [Google Scholar]
  183. 183. 
    Grassmann S, Pachmayr LO, Leube J, Mihatsch L, Andrae I et al. 2019. Distinct surface expression of activating receptor Ly49H drives differential expansion of NK cell clones upon murine cytomegalovirus infection. Immunity 50:61391–400.e4
    [Google Scholar]
  184. 184. 
    Karo JM, Schatz DG, Sun JC 2014. The RAG recombinase dictates functional heterogeneity and cellular fitness in natural killer cells. Cell 159:194–107
    [Google Scholar]
  185. 185. 
    Min-Oo G, Bezman NA, Madera S, Sun JC, Lanier LL 2014. Proapoptotic Bim regulates antigen-specific NK cell contraction and the generation of the memory NK cell pool after cytomegalovirus infection. J. Exp. Med. 211:71289–96
    [Google Scholar]
  186. 186. 
    Firth MA, Madera S, Beaulieu AM, Gasteiger G, Castillo EF et al. 2013. Nfil3-independent lineage maintenance and antiviral response of natural killer cells. J. Exp. Med. 210:132981–90
    [Google Scholar]
  187. 187. 
    O'Leary JG, Goodarzi M, Drayton DL, von Andrian UH 2006. T cell- and B cell-independent adaptive immunity mediated by natural killer cells. Nat. Immunol 7:5507–16
    [Google Scholar]
  188. 188. 
    Paust S, Gill HS, Wang B-Z, Flynn MP, Moseman EA et al. 2010. Critical role for the chemokine receptor CXCR6 in NK cell-mediated antigen-specific memory of haptens and viruses. Nat. Immunol. 11:121127–35
    [Google Scholar]
  189. 189. 
    Peng H, Jiang X, Chen Y, Sojka DK, Wei H et al. 2013. Liver-resident NK cells confer adaptive immunity in skin-contact inflammation. J. Clin. Investig. 123:41444–56
    [Google Scholar]
  190. 190. 
    Dou Y, Fu B, Sun R, Li W, Hu W et al. 2015. Influenza vaccine induces intracellular immune memory of human NK cells. PLOS ONE 10:3e0121258
    [Google Scholar]
  191. 191. 
    Suliman S, Geldenhuys H, Johnson JL, Hughes JE, Smit E et al. 2016. Bacillus Calmette-Guérin (BCG) revaccination of adults with latent Mycobacterium tuberculosis infection induces long-lived BCG-reactive NK cell responses. J. Immunol. 197:41100–10
    [Google Scholar]
  192. 192. 
    Nikzad R, Angelo LS, Aviles-Padilla K, Le DT, Singh VK et al. 2019. Human natural killer cells mediate adaptive immunity to viral antigens. Sci. Immunol. 4:35eaat8116
    [Google Scholar]
  193. 193. 
    Reeves RK, Li H, Jost S, Blass E, Li H et al. 2015. Antigen-specific NK cell memory in rhesus macaques. Nat. Immunol. 16:9927–32
    [Google Scholar]
  194. 194. 
    Sun JC, Beilke JN, Bezman NA, Lanier LL 2011. Homeostatic proliferation generates long-lived natural killer cells that respond against viral infection. J. Exp. Med. 208:2357–68
    [Google Scholar]
  195. 195. 
    Cooper MA, Elliott JM, Keyel PA, Yang L, Carrero JA, Yokoyama WM 2009. Cytokine-induced memory-like natural killer cells. PNAS 106:61915–19
    [Google Scholar]
  196. 196. 
    Martinez-Gonzalez I, Mathä L, Steer CA, Ghaedi M, Poon GFT, Takei F 2016. Allergen-experienced group 2 innate lymphoid cells acquire memory-like properties and enhance allergic lung inflammation. Immunity 45:1198–208
    [Google Scholar]
  197. 197. 
    Romee R, Schneider SE, Leong JW, Chase JM, Keppel CR et al. 2012. Cytokine activation induces human memory-like NK cells. Blood 120:244751–60
    [Google Scholar]
  198. 198. 
    Romee R, Rosario M, Berrien-Elliott MM, Wagner JA, Jewell BA et al. 2016. Cytokine-induced memory-like natural killer cells exhibit enhanced responses against myeloid leukemia. Sci. Transl. Med. 8:357357ra123
    [Google Scholar]
  199. 199. 
    Uppendahl LD, Felices M, Bendzick L, Ryan C, Kodal B et al. 2019. Cytokine-induced memory-like natural killer cells have enhanced function, proliferation, and in vivo expansion against ovarian cancer cells. Gynecol. Oncol. 153:1149–57
    [Google Scholar]
  200. 200. 
    Leong JW, Chase JM, Romee R, Schneider SE, Sullivan RP et al. 2014. Preactivation with IL-12, IL-15, and IL-18 induces CD25 and a functional high-affinity IL-2 receptor on human cytokine-induced memory-like natural killer cells. Biol. Blood Marrow Transplant. 20:4463–73
    [Google Scholar]
  201. 201. 
    Bigley AB, Baker FL, Simpson RJ 2018. Cytomegalovirus: an unlikely ally in the fight against blood cancers. ? Clin. Exp. Immunol. 193:3265–74
    [Google Scholar]
  202. 202. 
    Monaco EL, Tremante E, Cerboni C, Melucci E, Sibilio L et al. 2011. Human leukocyte antigen E contributes to protect tumor cells from lysis by natural killer cells. Neoplasia 13:9822–30
    [Google Scholar]
  203. 203. 
    Bigley AB, Rezvani K, Shah N, Sekine T, Balneger N et al. 2016. Latent cytomegalovirus infection enhances anti‐tumour cytotoxicity through accumulation of NKG2C+ NK cells in healthy humans. Clin. Exp. Immunol. 185:2239–51
    [Google Scholar]
  204. 204. 
    Cichocki F, Taras E, Chiuppesi F, Wagner JE, Blazar BR et al. 2019. Adaptive NK cell reconstitution is associated with better clinical outcomes. JCI Insight 4:2e125553
    [Google Scholar]
  205. 205. 
    Cichocki F, Cooley S, Davis Z, DeFor TE, Schlums H et al. 2016. CD56dimCD57+NKG2C+ NK cell expansion is associated with reduced leukemia relapse after reduced intensity HCT. Leukemia 30:2456–63
    [Google Scholar]
  206. 206. 
    Ito S, Pophali P, Wu CO, Koklanaris EK, Superata J et al. 2013. CMV reactivation is associated with a lower incidence of relapse after allo-SCT for CML. Bone Marrow Transplant. 48:101313–16
    [Google Scholar]
  207. 207. 
    Liu LL, Béziat V, Oei VYS, Pfefferle A, Schaffer M et al. 2017. Ex vivo expanded adaptive NK cells effectively kill primary acute lymphoblastic leukemia cells. Cancer Immunol. Res. 5:8654–65
    [Google Scholar]
  208. 208. 
    Béziat V, Dalgard O, Asselah T, Halfon P, Bedossa P et al. 2012. CMV drives clonal expansion of NKG2C+ NK cells expressing self‐specific KIRs in chronic hepatitis patients. Eur. J. Immunol. 42:2447–57
    [Google Scholar]
  209. 209. 
    Santomasso B, Bachier C, Westin J, Rezvani K, Shpall EJ 2019. The other side of CAR T-cell therapy: cytokine release syndrome, neurologic toxicity, and financial burden. Am. Soc. Clin. Oncol. Educ. Book 39:433–44
    [Google Scholar]
  210. 210. 
    Pfefferle A, Huntington ND. 2020. You have got a fast CAR: chimeric antigen receptor NK cells in cancer therapy. Cancers 12:3706
    [Google Scholar]
  211. 211. 
    Liu E, Marin D, Banerjee P, Macapinlac HA, Thompson P et al. 2020. Use of CAR-transduced natural killer cells in CD19-positive lymphoid tumors. N. Engl. J. Med. 382:6545–53
    [Google Scholar]
  212. 212. 
    Gang M, Marin ND, Wong P, Neal CC, Marsala L et al. 2020. CAR-modified memory-like NK cells exhibit potent responses to NK-resistant lymphomas. Blood 136:202308–18
    [Google Scholar]
  213. 213. 
    Restifo NP, Smyth MJ, Snyder A 2016. Acquired resistance to immunotherapy and future challenges. Nat. Rev. Cancer 16:2121–26
    [Google Scholar]
  214. 214. 
    André P, Denis C, Soulas C, Bourbon-Caillet C, Lopez J et al. 2018. Anti-NKG2A mAb is a checkpoint inhibitor that promotes anti-tumor immunity by unleashing both T and NK cells. Cell 175:71731–43.e13
    [Google Scholar]
  215. 215. 
    Pende D, Falco M, Vitale M, Cantoni C, Vitale C et al. 2019. Killer Ig-like receptors (KIRs): their role in NK cell modulation and developments leading to their clinical exploitation. Front. Immunol. 10:1179
    [Google Scholar]
  216. 216. 
    Bagot M, Porcu P, Marie-Cardine A, Battistella M, William BM et al. 2019. IPH4102, a first-in-class anti-KIR3DL2 monoclonal antibody, in patients with relapsed or refractory cutaneous T-cell lymphoma: an international, first-in-human, open-label, phase 1 trial. Lancet Oncol. 20:81160–70
    [Google Scholar]
  217. 217. 
    Vey N, Karlin L, Sadot-Lebouvier S, Broussais F, Berton-Rigaud D et al. 2018. A phase 1 study of lirilumab (antibody against killer immunoglobulin-like receptor antibody KIR2D; IPH2102) in patients with solid tumors and hematologic malignancies. Oncotarget 9:2517675–88
    [Google Scholar]
  218. 218. 
    Paolino M, Choidas A, Wallner S, Pranjic B, Uribesalgo I et al. 2014. The E3 ligase Cbl-b and TAM receptors regulate cancer metastasis via natural killer cells. Nature 507:7493508–12
    [Google Scholar]
  219. 219. 
    Delconte RB, Kolesnik TB, Dagley LF, Rautela J, Shi W et al. 2016. CIS is a potent checkpoint in NK cell-mediated tumor immunity. Nat. Immunol. 17:7816–24
    [Google Scholar]
  220. 220. 
    Miller JS, Lanier LL. 2019. Natural killer cells in cancer immunotherapy. Annu. Rev. Cancer Biol. 3:77–103
    [Google Scholar]
  221. 221. 
    Foster SL, Hargreaves DC, Medzhitov R 2007. Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 447:7147972–78
    [Google Scholar]
  222. 222. 
    Saeed S, Quintin J, Kerstens HHD, Rao NA, Aghajanirefah A et al. 2014. Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity. Science 345:62041251086
    [Google Scholar]
  223. 223. 
    Naik S, Larsen SB, Gomez NC, Alaverdyan K, Sendoel A et al. 2017. Inflammatory memory sensitizes skin epithelial stem cells to tissue damage. Nature 550:7677475–80
    [Google Scholar]
  224. 224. 
    Ordovas-Montanes J, Dwyer DF, Nyquist SK, Buchheit KM, Vukovic M et al. 2018. Allergic inflammatory memory in human respiratory epithelial progenitor cells. Nature 560:7720649–54
    [Google Scholar]
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