NK cells in host responses to viral infections

Current Opinion in Immunology

Volumn 44, Issue , 2017, Pages 43-51

  Lam, Viola C ^a,b   Lanier, Lewis L ^b,c  

^a Biomedical Sciences Graduate Program   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c PARKER INSTITUTE FOR CANCER IMMUNOTHERAPY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 15; INTERLEUKIN 18; CYTOKINE;

ADAPTIVE IMMUNITY; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INTERACTION; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CYTOKINE RELEASE; CYTOMEGALOVIRUS INFECTION; DENDRITIC CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; INFLUENZA; INNATE IMMUNITY; MEMORY CELL; NATURAL KILLER CELL; NONHUMAN; PROTEIN EXPRESSION; REVIEW; T LYMPHOCYTE ACTIVATION; VIRUS INFECTION; VIRUS REPLICATION; ANIMAL; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE SUBPOPULATION; METABOLISM;

ADAPTIVE IMMUNITY; ANIMALS; CYTOKINES; HUMANS; IMMUNITY, INNATE; IMMUNOLOGIC MEMORY; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; LYMPHOCYTE SUBSETS; VIRUS DISEASES;

EID: 85003816176     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2016.11.003     Document Type: Review

References (97)

1. 1 Biron, C.A., Byron, K.S., Sullivan, J.L., Severe herpesvirus infections in an adolescent without natural killer cells. N Engl J Med 320 (1989), 1731–1735.
2. 2 Notarangelo, L.D., Mazzolari, E., Natural killer cell deficiencies and severe varicella infection. J Pediatr 148 (2006), 563–564.
3. 3 Orange, J.S., Human natural killer cell deficiencies and susceptibility to infection. Microbes Infect Inst Pasteur 4 (2002), 1545–1558.
4. 4 Mace, E.M., Hsu, A.P., Monaco-Shawver, L., Makedonas, G., Rosen, J.B., Dropulic, L., Cohen, J.I., Frenkel, E.P., Bagwell, J.C., Sullivan, J.L., et al. Mutations in GATA2 cause human NK cell deficiency with specific loss of the CD56(bright) subset. Blood 121 (2013), 2669–2677.
5. 5 Lanier, L.L., Phillips, J.H., Hackett, J., Tutt, M., Kumar, V., Natural killer cells: definition of a cell type rather than a function. J Immunol 137 (1986), 2735–2739.
6. 6 O'Sullivan, T.E., Sun, J.C., Lanier, L.L., Natural killer cell memory. Immunity 43 (2015), 634–645.
7. 7 Cerwenka, A., Lanier, L.L., Natural killer cell memory in infection, inflammation and cancer. Nat Rev Immunol 16 (2016), 112–123.
8. 8 O'Leary, J.G., Goodarzi, M., Drayton, D.L., von Andrian, U.H., T cell- and B cell-independent adaptive immunity mediated by natural killer cells. Nat Immunol 7 (2006), 507–516.
9. 9 Paust, S., Gill, H.S., Wang, B.Z., Flynn, M.P., Moseman, E.A., Senman, B., Szczepanik, M., Telenti, A., Askenase, P.W., Compans, R.W., von Andrian, U.H., Critical role for the chemokine receptor CXCR6 in NK cell-mediated antigen-specific memory of haptens and viruses. Nat Immunol 11 (2010), 1127–1135.
10. 10 Cooper, M.A., Elliott, J.M., Keyel, P.A., Yang, L., Carrero, J.A., Yokoyama, W.M., Cytokine-induced memory-like natural killer cells. Proc Natl Acad Sci USA 106 (2009), 1915–1919.
11. 11 Prlic, M., Blazar, B.R., Farrar, M.A., Jameson, S.C., In vivo survival and homeostatic proliferation of natural killer cells. J Exp Med 197 (2003), 967–976.
12. − NK cells in response to alloantigen stimulation.
13. 13 Sun, J.C., Beilke, J.N., Lanier, L.L., Adaptive immune features of natural killer cells. Nature 457 (2009), 557–561.
14. 14 Hendricks, D.W., Min-Oo, G., Lanier, L.L., Sweet is the memory of past troubles: NK cells remember. Curr Top Microbiol Immunol 395 (2016), 147–171.
15. 15 Arase, H., Mocarski, E.S., Campbell, A.E., Hill, A.B., Lanier, L.L., Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296 (2002), 1323–1326.
16. 16 Daniels, K.A., Devora, G., Lai, W.C., O'Donnell, C.L., Bennett, M., Welsh, R.M., Murine cytomegalovirus is regulated by a discrete subset of natural killer cells reactive with monoclonal antibody to Ly49H. J Exp Med 194 (2001), 29–44.
17. 17 Smith, H.R.C., Heusel, J.W., Mehta, I.K., Kim, S., Dorner, B.G., Naidenko, O.V., Iizuka, K., Furukawa, H., Beckman, D.L., Pingel, J.T., et al. Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc Natl Acad Sci USA 99 (2002), 8826–8831.
18. + memory NK cells.
19. ••] demonstrates that Ly49C restricts NK cell control of MCMV.
20. ••] demonstrates that Ly49C restricts NK cell control of MCMV.
21. + NK cells restricts MCMV control.
22. 22 Abdul-Careem, M.F., Lee, A.J., Pek, E.A., Gill, N., Gillgrass, A.E., Chew, M.V., Reid, S., Ashkar, A.A., Genital HSV-2 infection induces short-term NK cell memory. PLoS ONE, 7, 2012, e32821.
23. 23 Gillard, G.O., Bivas-Benita, M., Hovav, A.H., Grandpre, L.E., Panas, M.W., Seaman, M.S., Haynes, B.F., Letvin, N.K., Thy1+ NK cells from vaccinia virus-primed mice confer protection against vaccinia virus challenge in the absence of adaptive lymphocytes. PLoS Pathog, 7, 2011, e1002141.
24. 24 van Helden, M.J.G., Zaiss, D.M.W., Sijts, A.J.A.M., CCR2 defines a distinct population of NK cells and mediates their migration during influenza virus infection in mice. PLoS ONE, 7, 2012, e52027.
25. 25• Reeves, R.K., Li, H., Jost, S., Blass, E., Li, H., Schafer, J.L., Varner, V., Manickam, C., Eslamizar, L., Altfeld, M., et al. Antigen-specific NK cell memory in rhesus macaques. Nat Immunol 16 (2015), 927–932 Demonstrates the persistence of SIV-specific memory NK cells from vaccination and viral infection.
26. 26 Giavedoni, L.D., Velasquillo, M.C., Parodi, L.M., Hubbard, G.B., Hodara, V.L., Cytokine expression, natural killer cell activation, and phenotypic changes in lymphoid cells from rhesus macaques during acute infection with pathogenic simian immunodeficiency virus. J Virol 74 (2000), 1648–1657.
27. 27 Gumá, M., Angulo, A., Vilches, C., Gómez-Lozano, N., Malats, N., López-Botet, M., Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood 104 (2004), 3664–3671.
28. 28 Gumá, M., Budt, M., Sáez, A., Brckalo, T., Hengel, H., Angulo, A., López-Botet, M., Expansion of CD94/NKG2C+ NK cells in response to human cytomegalovirus-infected fibroblasts. Blood 107 (2006), 3624–3631.
29. +NKG2Chi natural killer cell subset during acute human cytomegalovirus infection. Proc Natl Acad Sci USA 108 (2011), 14725–14732.
30. 30 Petitdemange, C., Becquart, P., Wauquier, N., Béziat, V., Debré, P., Leroy, E.M., Vieillard, V., Unconventional repertoire profile is imprinted during acute chikungunya infection for natural killer cells polarization toward cytotoxicity. PLoS Pathog, 7, 2011, e1002268.
31. 31 Béziat, V., Dalgard, O., Asselah, T., Halfon, P., Bedossa, P., Boudifa, A., Hervier, B., Theodorou, I., Martinot, M., Debré, P., et al. CMV drives clonal expansion of NKG2C+ NK cells expressing self-specific KIRs in chronic hepatitis patients. Eur J Immunol 42 (2012), 447–457.
32. 32 Saghafian-Hedengren, S., Sohlberg, E., Theorell, J., Carvalho-Queiroz, C., Nagy, N., Persson, J.O., Nilsson, C., Bryceson, Y.T., Sverremark-Ekström, E., Epstein-Barr virus coinfection in children boosts cytomegalovirus-induced differentiation of natural killer cells. J Virol 87 (2013), 13446–13455.
33. 33 Björkström, N.K., Lindgren, T., Stoltz, M., Fauriat, C., Braun, M., Evander, M., Michaëlsson, J., Malmberg, K.J., Klingström, J., Ahlm, C., Ljunggren, H.G., Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus. J Exp Med 208 (2011), 13–21.
34. 34 Björkström, N.K., Svensson, A., Malmberg, K.J., Eriksson, K., Ljunggren, H.G., Characterization of natural killer cell phenotype and function during recurrent human HSV-2 infection. PLoS ONE, 6, 2011, e27664.
35. + memory NK cells.
36. + NK cells is triggered by co-culture with HCMV-infected primary human endothelial cells.
37. 37 Rölle, A., Pollmann, J., Ewen, E.M., Le, V.T.K., Halenius, A., Hengel, H., Cerwenka, A., IL-12-producing monocytes and HLA-E control HCMV-driven NKG2C+ NK cell expansion. J Clin Invest 124 (2014), 5305–5316.
38. ••] identifies synergy of CD2-mediated and CD16-mediated NK cell activation in HCMV infection.
39. ••] identifies synergy of CD2-mediated and CD16-mediated NK cell activation in HCMV infection.
40. 40 Rölle, A., Brodin, P., Immune adaptation to environmental influence: the case of NK cells and HCMV. Trends Immunol 37 (2016), 233–243.
41. 41 Mócsai, A., Diverse novel functions of neutrophils in immunity, inflammation, and beyond. J Exp Med 210 (2013), 1283–1299.
42. 42 Scapini, P., Cassatella, M.A., Social networking of human neutrophils within the immune system. Blood 124 (2014), 710–719.
43. 43 Costantini, C., Micheletti, A., Calzetti, F., Perbellini, O., Pizzolo, G., Cassatella, M.A., Neutrophil activation and survival are modulated by interaction with NK cells. Int Immunol 22 (2010), 827–838.
44. 44 Thorén, F.B., Riise, R.E., Ousbäck, J., Della Chiesa, M., Alsterholm, M., Marcenaro, E., Pesce, S., Prato, C., Cantoni, C., Bylund, J., Human, N.K., et al. Cells induce neutrophil apoptosis via an NKp46- and Fas-dependent mechanism. J Immunol 188 (2012), 1668–1674.
45. 45 Stacey, M.A., Marsden, M., Pham, N.T.A., Clare, S., Dolton, G., Stack, G., Jones, E., Klenerman, P., Gallimore, A.M., Taylor, P.R., et al. Neutrophils recruited by IL-22 in peripheral tissues function as TRAIL-dependent antiviral effectors against MCMV. Cell Host Microbe 15 (2014), 471–483.
46. 46 Jaeger, B.N., Donadieu, J., Cognet, C., Bernat, C., Ordoñez-Rueda, D., Barlogis, V., Mahlaoui, N., Fenis, A., Narni-Mancinelli, E., Beaupain, B., et al. Neutrophil depletion impairs natural killer cell maturation, function, and homeostasis. J Exp Med 209 (2012), 565–580.
47. 47•• Riise, R.E., Bernson, E., Aurelius, J., Martner, A., Pesce, S., Della Chiesa, M., Marcenaro, E., Bylund, J., Hellstrand, K., Moretta, L., et al. TLR-stimulated neutrophils instruct NK cells to trigger dendritic cell maturation and promote adaptive T cell responses. J Immunol 195 (2015), 1121–1128 Illustrates the interaction between neutrophils and NK cells in coordinating an immune response.
48. 48• Pliyev, B.K., Kalintseva, M.V., Abdulaeva, S.V., Yarygin, K.N., Savchenko, V.G., Neutrophil microparticles modulate cytokine production by natural killer cells. Cytokine 65 (2014), 126–129 Demonstrates the effects of neutrophil microparticles on NK cells to produce anti-inflammatory cytokines.
49. 49• Amano, K., Hirayama, M., Azuma, E., Iwamoto, S., Keida, Y., Komada, Y., Neutrophils induced licensing of natural killer cells. Mediators Inflamm, 2015, 10.1155/2015/747680 Demonstrates the promotion of NK cell licensing by neutrophils.
50. 50 Michel, T., Hentges, F., Zimmer, J., Consequences of the crosstalk between monocytes/macrophages and natural killer cells. Front Immunol, 2012, 10.3389/fimmu.2012.00403.
51. 51 Romo, N., Magri, G., Muntasell, A., Heredia, G., Baía, D., Angulo, A., Guma, M., López-Botet, M., Natural killer cell-mediated response to human cytomegalovirus-infected macrophages is modulated by their functional polarization. J Leukoc Biol 90 (2011), 717–726.
52. 52 Bellora, F., Castriconi, R., Dondero, A., Reggiardo, G., Moretta, L., Mantovani, A., Moretta, A., Bottino, C., The interaction of human natural killer cells with either unpolarized or polarized macrophages results in different functional outcomes. Proc Natl Acad Sci USA 107 (2010), 21659–21664.
53. 53•• Lenac Rovis, T., Kucan Brlic, P., Kaynan, N., Juranic Lisnic, V., Brizic, I., Jordan, S., Tomic, A., Kvestak, D., Babic, M., Tsukerman, P., et al. Inflammatory monocytes and NK cells play a crucial role in DNAM-1-dependent control of cytomegalovirus infection. J Exp Med 213 (2016), 1835–1850 Identifies DNAM-1 as a critical component of monocyte and NK cell interactions during MCMV infection.
54. 54• Quillay, H., El Costa, H., Duriez, M., Marlin, R., Cannou, C., Madec, Y., de Truchis, C., Rahmati, M., Barré-Sinoussi, F., Nugeyre, M.T., Menu, E., NK cells control HIV-1 infection of macrophages through soluble factors and cellular contacts in the human decidua. Retrovirology, 2016, 10.1186/s12977-016-0271-z Demonstrates control of HIV-1 in decidual macrophages by NK cells.
55. 55 Ferlazzo, G., Pack, M., Thomas, D., Paludan, C., Schmid, D., Strowig, T., Bougras, G., Muller, W.A., Moretta, L., Münz, C., Distinct roles of IL-12 and IL-15 in human natural killer cell activation by dendritic cells from secondary lymphoid organs. Proc Natl Acad Sci USA 101 (2004), 16606–16611.
56. 56 Vitale, M., Della Chiesa, M., Carlomagno, S., Romagnani, C., Thiel, A., Moretta, L., Moretta, A., The small subset of CD56brightCD16- natural killer cells is selectively responsible for both cell proliferation and interferon-gamma production upon interaction with dendritic cells. Eur J Immunol 34 (2004), 1715–1722.
57. 57 Vitale, M., Della Chiesa, M., Carlomagno, S., Pende, D., Aricò, M., Moretta, L., Moretta, A., NK-dependent DC maturation is mediated by TNFalpha and IFNgamma released upon engagement of the NKp30 triggering receptor. Blood 106 (2005), 566–571.
58. 58 Mortier, E., Woo, T., Advincula, R., Gozalo, A., Ma, A., IL-15Ralpha chaperones IL-15 to stable dendritic cell membrane complexes that activate NK cells via trans presentation. J Exp Med 205 (2008), 1213–1225.
59. 59 Moretta, A., Natural killer cells and dendritic cells: rendezvous in abused tissues. Nat Rev Immunol 2 (2002), 957–964.
60. 60 Fehniger, T.A., Cooper, M.A., Nuovo, G.J., Cella, M., Facchetti, F., Colonna, M., Caligiuri, M.A., CD56bright natural killer cells are present in human lymph nodes and are activated by T cell-derived IL-2: a potential new link between adaptive and innate immunity. Blood 101 (2003), 3052–3057.
61. 61 Martín-Fontecha, A., Thomsen, L.L., Brett, S., Gerard, C., Lipp, M., Lanzavecchia, A., Sallusto, F., Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol 5 (2004), 1260–1265.
62. 62• Lawler, C., Tan, C.S.E., Simas, J.P., Stevenson, P.G., Type 1 interferons and NK cells restrict gamma-herpesvirus lymph node infection. J Virol, 2016, 10.1128/JVI.01108-16 Illustrates the importance of NK cell recruitment to the lymph node during viral infection.
63. 63 Mailliard, R.B., Son, Y.I., Redlinger, R., Coates, P.T., Giermasz, A., Morel, P.A., Storkus, W.J., Kalinski, P., Dendritic cells mediate NK cell help for Th1 and CTL responses: two-signal requirement for the induction of NK cell helper function. J Immunol 171 (2003), 2366–2373.
64. 64 Morandi, B., Bougras, G., Muller, W.A., Ferlazzo, G., Münz, C., NK cells of human secondary lymphoid tissues enhance T cell polarization via IFN-gamma secretion. Eur J Immunol 36 (2006), 2394–2400.
65. 65 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 195 (2002), 327–333.
66. 66 Goldszmid, R.S., Caspar, P., Rivollier, A., White, S., Dzutsev, A., Hieny, S., Kelsall, B., Trinchieri, G., Sher, A., NK cell-derived interferon-γ orchestrates cellular dynamics and the differentiation of monocytes into dendritic cells at the site of infection. Immunity 36 (2012), 1047–1059.
67. 67•• Vogel, K., Thomann, S., Vogel, B., Schuster, P., Schmidt, B., Both plasmacytoid dendritic cells and monocytes stimulate natural killer cells early during human herpes simplex virus type 1 infections. Immunology 143 (2014), 588–600 With Ref. [68] demonstrates NK cell activation by herpes simplex virus-exposed dendritic cells.
68. 68 Swiecki, M., Wang, Y., Gilfillan, S., Colonna, M., Plasmacytoid dendritic cells contribute to systemic but not local antiviral responses to HSV infections. PLoS Pathog, 9, 2013, e1003728.
69. 69• Brandstadter, J.D., Huang, X., Yang, Y., NK cell-extrinsic IL-18 signaling is required for efficient NK-cell activation by vaccinia virus. Eur J Immunol 44 (2014), 2659–2666 Demonstrates IL-18 signaling and NKG2D engagement from dendritic cells are required for NK cell-mediated control of vaccinia virus.
70. + T cells. Eur J Immunol 44 (2014), 2370–2379 Demonstrates activation of NK cells with HIV-1-infected dendritic cells requires IL-15 signaling and NKG2D engagement.
71. 71 Chang, M.O., Suzuki, T., Suzuki, H., Takaku, H., HIV-1 Gag-virus-like particles induce natural killer cell immune responses via activation and maturation of dendritic cells. J Innate Immun 4 (2012), 187–200.
72. 72 Pende, D., Castriconi, R., Romagnani, P., Spaggiari, G.M., Marcenaro, S., Dondero, A., Lazzeri, E., Lasagni, L., Martini, S., River, P., et al. Expression of the DNAM-1 ligands, Nectin-2 (CD112) and poliovirus receptor (CD155), on dendritic cells: relevance for natural killer-dendritic cell interaction. Blood 107 (2006), 2030–2036.
73. 73• Smith, L.E., Olszewski, M.A., Georgoudaki, A.M., Wagner, A.K., Hägglöf, T., Karlsson, M.C.I., Dominguez-Villar, M., Garcia-Cozar, F., Mueller, S., Ravens, I., et al. Sensitivity of dendritic cells to NK-mediated lysis depends on the inflammatory environment and is modulated by CD54/CD226-driven interactions. J Leukoc Biol, 2016, 10.1189/jlb.3A0615-271RR Demonstrates lysis of GM-CSF activated dendritic cells by NK cells is mediated by DNAM-1 and LFA-1.
74. 74 Elboim, M., Grodzovski, I., Djian, E., Wolf, D.G., Mandelboim, O., HSV-2 specifically down regulates HLA-C expression to render HSV-2-infected DCs susceptible to NK cell killing. PLoS Pathog, 9, 2013, e1003226.
75. 75• Lim, D.S.L., Yawata, N., Selva, K.J., Li, N., Tsai, C.Y., Yeong, L.H., Liong, K.H., Ooi, E.E., Chong, N.K., Ng, M.L., et al. The combination of type I IFN, TNF-α, and cell surface receptor engagement with dendritic cells enables NK cells to overcome immune evasion by dengue virus. J Immunol 193 (2014), 5065–5075 Demonstrates cytokine-dependent and contact-dependent interactions between dendritic cells and NK cells in response to Dengue virus infection.
76. 76 Martinet, J., Dufeu-Duchesne, T., Bruder Costa, J., Larrat, S., Marlu, A., Leroy, V., Plumas, J., Aspord, C., Altered functions of plasmacytoid dendritic cells and reduced cytolytic activity of natural killer cells in patients with chronic HBV infection. Gastroenterology 143 (2012), 1586–1596.
77. 77 Tjwa, E.T.T.L., van Oord, G.W., Biesta, P.J., Boonstra, A., Janssen, H.L.A., Woltman, A.M., Restoration of TLR3-activated myeloid dendritic cell activity leads to improved natural killer cell function in chronic hepatitis B virus infection. J Virol 86 (2012), 4102–4109.
78. 78 Mandaric, S., Walton, S.M., Rülicke, T., Richter, K., Girard-Madoux, M.J.H., Clausen, B.E., Zurunic, A., Kamanaka, M., Flavell, R.A., Jonjic, S., Oxenius, A., IL-10 suppression of NK/DC crosstalk leads to poor priming of MCMV-specific CD4 T cells and prolonged MCMV persistence. PLoS Pathog, 8, 2012, e1002846.
79. 79•• Ellegård, R., Crisci, E., Andersson, J., Shankar, E.M., Nyström, S., Hinkula, J., Larsson, M., Impaired NK cell activation and chemotaxis toward dendritic cells exposed to complement-opsonized HIV-1. J Immunol 195 (2015), 1698–1704 Illustrates impaired NK cell recruitment by dendritic cells exposed to complement-opsonized HIV-1 virus.
80. 80 Su, H.C., Nguyen, K.B., Salazar-Mather, T.P., Ruzek, M.C., Dalod, M.Y., Biron, C.A., NK cell functions restrain T cell responses during viral infections. Eur J Immunol 31 (2001), 3048–3055.
81. 81 Krebs, P., Barnes, M.J., Lampe, K., Whitley, K., Bahjat, K.S., Beutler, B., Janssen, E., Hoebe, K., NK-cell-mediated killing of target cells triggers robust antigen-specific T-cell-mediated and humoral responses. Blood 113 (2009), 6593–6602.
82. 82 Cook, K.D., Waggoner, S.N., Whitmire, J.K., NK cells and their ability to modulate T cells during virus infections. Crit Rev Immunol 34 (2014), 359–388.
83. 83 Waggoner, S.N., Cornberg, M., Selin, L.K., Welsh, R.M., Natural killer cells act as rheostats modulating antiviral T cells. Nature 481 (2012), 394–398.
84. ••] demonstrates dual functions of NK cells in controlling T cell responses in lymphocytic choriomeningitis virus infection.
85. + T cell generation due to chronic lymphocytic choriomeningitis virus infection.
86. 86 Cook, K.D., Whitmire, J.K., The depletion of NK cells prevents T cell exhaustion to efficiently control disseminating virus infection. J Immunol 190 (2013), 641–649.
87. •,86] demonstrates dual functions of NK cells in controlling T cell responses in lymphocytic choriomeningitis virus infection.
88. + T cells protects against NK cell-mediated lysis.
89. + T cell priming and dendritic cell migration during influenza A infection by IFN-γ and perforin-dependent mechanisms. J Immunol 189 (2012), 2099–2109.
90. 90 Abdul-Careem, M.F., Mian, M.F., Yue, G., Gillgrass, A., Chenoweth, M.J., Barra, N.G., Chew, M.V., Chan, T., Al-Garawi, A.A., Jordana, M., Ashkar, A.A., Critical role of natural killer cells in lung immunopathology during influenza infection in mice. J Infect Dis 206 (2012), 167–177.
91. 91 Kim, M., Osborne, N.R., Zeng, W., Donaghy, H., McKinnon, K., Jackson, D.C., Cunningham, A.L., Herpes simplex virus antigens directly activate NK cells via TLR2, thus facilitating their presentation to CD4 T lymphocytes. J Immunol 188 (2012), 4158–4170.
92. + T cells.
93. + T cell cooperative immune responses correlate with control of disease in a macaque simian immunodeficiency virus infection model. J Immunol 189 (2012), 1878–1885.
94. + T cells to induce NK cell effector functions.
95. + T-cell response. J Virol 86 (2012), 2165–2175.
96. + T cells and NK cells.
97. + T cells.