Licensed and unlicensed NK cells: Differential roles in cancer and viral control

Frontiers in Immunology

Volumn 7, Issue MAY, 2016, Pages

  Tu, Megan M ^a   Mahmoud, Ahmad Bakur ^a,b   Makrigiannis, Andrew P ^a,c  

^a UNIVERSITY OF OTTAWA   (Canada)

^b TAIBAH UNIVERSITY   (Saudi Arabia)

^c DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Immunity; Licensing; Ly49; MHC I; NK cells

Indexed keywords

KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL1; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL2; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL3; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DS1; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DS2; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DS4; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 3DL1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY A; POLYINOSINIC POLYCYTIDYLIC ACID; UNCLASSIFIED DRUG;

ACUTE MYELOBLASTIC LEUKEMIA; ANTIGEN RECOGNITION; CANCER CONTROL; CELL FUNCTION; CELL MATURATION; CHEDIAK HIGASHI SYNDROME; CLINICAL TRIAL (TOPIC); DISEASE MODEL; GENE; HODGKIN DISEASE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HYPOTHESIS; IMMUNOSURVEILLANCE; MOLECULAR MIMICRY; MULTIPLE MYELOMA; NATURAL KILLER T CELL; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); REVIEW; T LYMPHOCYTE SUBPOPULATION; TUMOR ESCAPE; VIRUS IMMUNITY;

EID: 84973548554     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00166     Document Type: Review

References (107)

1. Kiessling R, Klein E, Wigzell H. '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 (1975) 5:112-7. doi: 10.1002/eji.1830050208
2. Herberman RB, Nunn ME, Lavrin DH. Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic and allogeneic tumors. I. Distribution of reactivity and specificity. Int J Cancer (1975) 16:216-29. doi:10.1002/ijc.2910160205
3. Lanier LL. NK cell recognition. Annu Rev Immunol (2005) 23:225-74. doi:10.1146/annurev.immunol.23.021704.115526
4. Biron CA, Byron KS, Sullivan JL. Severe herpesvirus infections in an adolescent without natural killer cells. N Engl J Med (1989) 320:1731-5. doi:10.1056/NEJM198906293202605
5. Akiba H, Motoki Y, Satoh M, Iwatsuki K, Kaneko F. Recalcitrant trichophytic granuloma associated with NK-cell deficiency in a SLE patient treated with corticosteroid. Eur J Dermatol (2001) 11:58-62
6. Ballas ZK, Turner JM, Turner DA, Goetzman EA, Kemp JD. A patient with simultaneous absence of "classical" natural killer cells (CD3-, CD16+, and NKH1+) and expansion of CD3+, CD4-, CD8-, NKH1+ subset. J Allergy Clin Immunol (1990) 85:453-9. doi:10.1016/0091-6749(90)90155-W
7. Bernard F, Picard C, Cormier-Daire V, Eidenschenk C, Pinto G, Bustamante JC, et al. A novel developmental and immunodeficiency syndrome associated with intrauterine growth retardation and a lack of natural killer cells. Pediatrics (2004) 113:136-41. doi:10.1542/peds.113.1.136
8. Eidenschenk C, Dunne J, Jouanguy E, Fourlinnie C, Gineau L, Bacq D, et al. A novel primary immunodeficiency with specific natural-killer cell deficiency maps to the centromeric region of chromosome 8. Am J Hum Genet (2006) 78:721-7. doi:10.1086/503269
9. Etzioni A, Eidenschenk C, Katz R, Beck R, Casanova JL, Pollack S. Fatal varicella associated with selective natural killer cell deficiency. J Pediatr (2005) 146:423-5. doi:10.1016/j.jpeds.2004.11.022
10. Notarangelo LD, Mazzolari E. Natural killer cell deficiencies and severe varicella infection. J Pediatr (2006) 148:563-4. doi:10.1016/j.jpeds.2005.06.028 author reply 564
11. Wendland T, Herren S, Yawalkar N, Cerny A, Pichler WJ. Strong alpha beta and gamma delta TCR response in a patient with disseminated Mycobacterium avium infection and lack of NK cells and monocytopenia. Immunol Lett (2000) 72:75-82. doi:10.1016/S0165-2478(00)00169-3
12. Shaw RK, Issekutz AC, Fraser R, Schmit P, Morash B, Monaco-Shawver L, et al. Bilateral adrenal EBV-associated smooth muscle tumors in a child with a natural killer cell deficiency. Blood (2012) 119:4009-12. doi:10.1182/blood-2011-10-385377
13. Strengell M, Matikainen S, Siren J, Lehtonen A, Foster D, Julkunen I, et al. IL-21 in synergy with IL-15 or IL-18 enhances IFN-gamma production in human NK and T cells. J Immunol (2003) 170:5464-9. doi:10.4049/jimmunol.170.11.5464
14. Vitale M, Della Chiesa M, Carlomagno S, Romagnani C, Thiel A, Moretta L, et al. 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 (2004) 34:1715-22. doi:10.1002/eji.200425100
15. Ferlazzo G, Pack M, Thomas D, Paludan C, Schmid D, Strowig T, et al. 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 U S A (2004) 101:16606-11. doi:10.1073/pnas.0407522101
16. Koka R, Burkett P, Chien M, Chai S, Boone DL, Ma A. Cutting edge: murine dendritic cells require IL-15R alpha to prime NK cells. J Immunol (2004) 173:3594-8. doi:10.4049/jimmunol.173.6.3594
17. Granucci F, Zanoni I, Pavelka N, Van Dommelen SL, Andoniou CE, Belardelli F, et al. A contribution of mouse dendritic cell-derived IL-2 for NK cell activation. J Exp Med (2004) 200:287-95. doi:10.1084/jem.20040370
18. Yokoyama WM, Kehn PJ, Cohen DI, Shevach EM. Chromosomal location of the Ly-49 (A1, YE1/48) multigene family: genetic association with the NK 1.1 antigen. J Immunol (1990) 145:2353-8
19. Daab AS, Fuggle SV, Fabre JW, Ting A, Morris PJ. The detailed distribution of HLA-A, B, C antigens in normal human organs. Transplantation (1984) 38:287-92. doi:10.1097/00007890-198409000-00018
20. Bukur J, Jasinski S, Seliger B. The role of classical and non-classical HLA class I antigens in human tumors. Semin Cancer Biol (2012) 22:350-8. doi:10.1016/j.semcancer.2012.03.003
21. Garcia KC, Degano M, Stanfield RL, Brunmark A, Jackson MR, Peterson PA, et al. An alphabeta T cell receptor structure at 2.5 A and its orientation in the TCR-MHC complex. Science (1996) 274:209-19. doi:10.1126/science.274.5285.209
22. Davis MM, Bjorkman PJ. T-cell antigen receptor genes and T-cell recognition. Nature (1988) 334:395-402. doi:10.1038/334395a0
23. Karre K, Ljunggren HG, Piontek G, Kiessling R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature (1986) 319:675-8. doi:10.1038/319675a0
24. Karlhofer FM, Ribaudo RK, Yokoyama WM. MHC class I alloantigen specificity of Ly-49+ IL-2-activated natural killer cells. Nature (1992) 358:66-70. doi:10.1038/358066a0
25. Restifo NP, Esquivel F, Kawakami Y, Yewdell JW, Mule JJ, Rosenberg SA, et al. Identification of human cancers deficient in antigen processing. J Exp Med (1993) 177:265-72. doi:10.1084/jem.177.2.265
26. Restifo NP, Marincola FM, Kawakami Y, Taubenberger J, Yannelli JR, Rosenberg SA. Loss of functional beta2-microglobulin in metastatic melanomas from five patients receiving immunotherapy. J Natl Cancer Inst (1996) 88:100-8. doi:10.1093/jnci/88.2.100
27. Stern P, Gidlund M, Orn A, Wigzell H. Natural killer cells mediate lysis of embryonal carcinoma cells lacking MHC. Nature (1980) 285:341-2. doi:10.1038/285341a0
28. Bix M, Liao NS, Zijlstra M, Loring J, Jaenisch R, Raulet D. Rejection of class I MHC-deficient haemopoietic cells by irradiated MHC-matched mice. Nature (1991) 349:329-31. doi:10.1038/349329a0
29. Harel-Bellan A, Quillet A, Marchiol C, DeMars R, Tursz T, Fradelizi D. Natural killer susceptibility of human cells may be regulated by genes in the HLA region on chromosome 6. Proc Natl Acad Sci U S A (1986) 83:5688-92. doi:10.1073/pnas.83.15.5688
30. Fernandez NC, Treiner E, Vance RE, Jamieson AM, Lemieux S, Raulet DH. A subset of natural killer cells achieves self-tolerance without expressing inhibitory receptors specific for self-MHC molecules. Blood (2005) 105:4416-23. doi:10.1182/blood-2004-08-3156
31. Kim S, Poursine-Laurent J, Truscott SM, Lybarger L, Song YJ, Yang L, et al. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature (2005) 436:709-13. doi:10.1038/nature03847
32. Liao NS, Bix M, Zijlstra M, Jaenisch R, Raulet D. MHC class I deficiency: susceptibility to natural killer (NK) cells and impaired NK activity. Science (1991) 253:199-202. doi:10.1126/science.1853205
33. Belanger S, Tu MM, Rahim MM, Mahmoud AB, Patel R, Tai LH, et al. Impaired natural killer cell self-education and "missing-self" responses in Ly49-deficient mice. Blood (2012) 120:592-602. doi:10.1182/blood-2012-02-408732
34. Brodin P, Lakshmikanth T, Johansson S, Karre K, Hoglund P. The strength of inhibitory input during education quantitatively tunes the functional responsiveness of individual natural killer cells. Blood (2009) 113:2434-41. doi:10.1182/blood-2008-05-156836
35. Joncker NT, Fernandez NC, Treiner E, Vivier E, Raulet DH. NK cell responsiveness is tuned commensurate with the number of inhibitory receptors for self-MHC class I: the rheostat model. J Immunol (2009) 182:4572-80. doi:10.4049/jimmunol.0803900
36. Anfossi N, André P, Guia S, Falk CS, Roetynck S, Stewart CA, et al. Human NK cell education by inhibitory receptors for MHC class I. Immunity (2006) 25:331-42. doi:10.1016/j.immuni.2006.06.013
37. Kim S, Sunwoo JB, Yang L, Choi T, Song YJ, French AR, et al. HLA alleles determine differences in human natural killer cell responsiveness and potency. Proc Natl Acad Sci U S A (2008) 105:3053-8. doi:10.1073/pnas.0712229105
38. Hoglund P, Brodin P. Current perspectives of natural killer cell education by MHC class I molecules. Nat Rev Immunol (2010) 10:724-34. doi:10.1038/nri2835
39. Elliott JM, Wahle JA, Yokoyama WM. MHC class I-deficient natural killer cells acquire a licensed phenotype after transfer into an MHC class I-sufficient environment. J Exp Med (2010) 207:2073-9. doi:10.1084/jem.20100986
40. Joncker NT, Shifrin N, Delebecque F, Raulet DH. Mature natural killer cells reset their responsiveness when exposed to an altered MHC environment. J Exp Med (2010) 207:2065-72. doi:10.1084/jem.20100570
41. Chalifour A, Scarpellino L, Back J, Brodin P, Devèvre E, Gros F, et al. A role for cis interaction between the inhibitory Ly49A receptor and MHC class I for natural killer cell education. Immunity (2009) 30:337-47. doi:10.1016/j.immuni.2008.12.019
42. Ortaldo JR, Mason AT, Winkler-Pickett R, Raziuddin A, Murphy WJ, Mason LH. Ly-49 receptor expression and functional analysis in multiple mouse strains. J Leukoc Biol (1999) 66:512-20
43. Kirk GD, Merlo C, O'Driscoll P, Mehta SH, Galai N, Vlahov D, et al. HIV infection is associated with an increased risk for lung cancer, independent of smoking. Clin Infect Dis (2007) 45:103-10. doi:10.1086/518606
44. Moloney FJ, Comber H, O'Lorcain P, O'Kelly P, Conlon PJ, Murphy GM. A population-based study of skin cancer incidence and prevalence in renal transplant recipients. Br J Dermatol (2006) 154:498-504. doi:10.1111/j.1365-2133.2005.07021.x
45. Jiang Y, Villeneuve PJ, Wielgosz A, Schaubel DE, Fenton SSA, Mao Y. The incidence of cancer in a population-based cohort of Canadian heart transplant recipients. Am J Transplant (2010) 10:637-45. doi:10.1111/j.1600-6143.2009.02973.x
46. Clemente CG, Mihm MC Jr, Bufalino R, Zurrida S, Collini P, Cascinelli N. Prognostic value of tumor infiltrating lymphocytes in the vertical growth phase of primary cutaneous melanoma. Cancer (1996) 77:1303-10. doi:10.1002/(SICI)1097-0142(19960401)77:7<1303::AID-CNCR12>3.3.CO;2-0
47. Roder J, Duwe A. The beige mutation in the mouse selectively impairs natural killer cell function. Nature (1979) 278:451-3. doi:10.1038/278451a0
48. Haliotis T, Ball JK, Dexter D, Roder JC. Spontaneous and induced primary oncogenesis in natural killer (NK)-cell-deficient beige mutant mice. Int J Cancer (1985) 35:505-13. doi:10.1002/ijc.2910350414
49. Efrati P, Jonas W. Chediak's anomaly of leukocytes in malignant lymphoma associated with leukemic manifestations: case report with necropsy. Blood (1958) 13:1063-73
50. Kritzler RA, Terner JY, Lindenbaum J, Magidson J, Williams R, Presig R, et al. Chediak-Higashi syndrome. Cytologic and serum lipid observations in a case and family. Am J Med (1964) 36:583-94. doi:10.1016/0002-9343(64)90106-8
51. Windhorst DB, Zelickson AS, Good RA. Chediak-Higashi syndrome: hereditary gigantism of cytoplasmic organelles. Science (1966) 151:81-3. doi:10.1126/science.151.3706.81
52. Roder JC, Haliotis T, Klein M, Korec S, Jett JR, Ortaldo J, et al. A new immunodeficiency disorder in humans involving NK cells. Nature (1980) 284:553-5. doi:10.1038/284553a0
53. Gorelik E, Wiltrout RH, Okumura K, Habu S, Herberman RB. Role of NK cells in the control of metastatic spread and growth of tumor cells in mice. Int J Cancer (1982) 30:107-12. doi:10.1002/ijc.2910300118
54. Lanier LL, Le AM, Civin CI, Loken MR, Phillips JH. The relationship of CD16 (Leu-11) and Leu-19 (NKH-1) antigen expression on human peripheral blood NK cells and cytotoxic T lymphocytes. J Immunol (1986) 136:4480-6
55. Pross HF, Lotzova E. Role of natural killer cells in cancer. Nat Immun (1993) 12:279-92
56. Imai K, Matsuyama S, Miyake S, Suga K, Nakachi K. Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet (2000) 356:1795-9. doi:10.1016/S0140-6736(00)03231-1
57. Komiyama A, Kawai H, Yamada S, Kato M, Yanagisawa M, Miyagawa Y, et al. A killing defect of natural killer cells with the absence of natural killer cytotoxic factors in a child with Hodgkin's disease. Blood (1987) 69:1686-90
58. Goepel JR, Rees RC, Rogers K, Stoddard CJ, Thomas WEG, Shephard L. Loss of monomorphic and polymorphic HLA antigens in metastatic breast and colon carcinoma. Br J Cancer (1991) 64:880-3. doi:10.1038/bjc.1991.418
59. McDougall CJ, Ngoi SS, Goldman IS, Godwin T, Felix J, DeCosse JJ, et al. Reduced expression of HLA class I and II antigens in colon cancer. Cancer Res (1990) 50:8023-7
60. Vitale M, Rezzani R, Rodella L, Zauli G, Grigolato P, Cadei M, et al. HLA class I antigen and transporter associated with antigen processing (TAP1 and TAP2) down-regulation in high-grade primary breast carcinoma lesions. Cancer Res (1998) 58:737-42
61. Cathro HP, Smolkin ME, Theodorescu D, Jo VY, Ferrone S, Frierson HF Jr. Relationship between HLA class i antigen processing machinery component expression and the clinicopathologic characteristics of bladder carcinomas. Cancer Immunol Immunother (2010) 59:465-72. doi:10.1007/s00262-009-0765-9
62. Han L, Fletcher MS, Urbauer DL, Mueller P, Landen CN, Kamat AA, et al. HLA class i antigen processing machinery component expression and intratumoral T-Cell infiltrate as independent prognostic markers in ovarian carcinoma. Clin Cancer Res (2008) 14:3372-9. doi:10.1158/1078-0432.CCR-07-4433
63. Mehta AM, Jordanova ES, Kenter GG, Ferrone S, Fleuren GJ. Association of antigen processing machinery and HLA class I defects with clinicopathological outcome in cervical carcinoma. Cancer Immunol Immunother (2008) 57:197-206. doi:10.1007/s00262-007-0362-8
64. Tu MM, Mahmoud AB, Wight A, Mottashed A, Belanger S, Rahim MM, et al. Ly49 family receptors are required for cancer immunosurveillance mediated by natural killer cells. Cancer Res (2014) 74:3684-94. doi:10.1158/0008-5472.CAN-13-3021
65. Koh CY, Blazar BR, George T, Welniak LA, Capitini CM, Raziuddin A, et al. Augmentation of antitumor effects by NK cell inhibitory receptor blockade in vitro and in vivo. Blood (2001) 97:3132-7. doi:10.1182/blood.V97.10.3132
66. Sun K, Alvarez M, Ames E, Barao I, Chen M, Longo DL, et al. Mouse NK cell-mediated rejection of bone marrow allografts exhibits patterns consistent with Ly49 subset licensing. Blood (2012) 119:1590-8. doi:10.1182/blood-2011-08-374314
67. Orr MT, Murphy WJ, Lanier LL. 'Unlicensed' natural killer cells dominate the response to cytomegalovirus infection. Nat Immunol (2010) 11:321-7. doi:10.1038/ni.1849
68. Romagné F, André P, Spee P, Zahn S, Anfossi N, Gauthier L, et al. Preclinical characterization of 1-7F9, a novel human anti-KIR receptor therapeutic antibody that augments natural killer-mediated killing of tumor cells. Blood (2009) 114:2667-77. doi:10.1182/blood-2009-02-206532
69. Benson DM Jr, Hofmeister CC, Padmanabhan S, Suvannasankha A, Jagannath S, Abonour R, et al. A phase 1 trial of the anti-KIR antibody IPH2101 in patients with relapsed/refractory multiple myeloma. Blood (2012) 120:4324-33. doi:10.1182/blood-2012-06-438028
70. Vey N, Bourhis JH, Boissel N, Bordessoule D, Prebet T, Charbonnier A, et al. A phase 1 trial of the anti-inhibitory KIR mAb IPH2101 for AML in complete remission. Blood (2012) 120:4317-23. doi:10.1182/blood-2012-06-437558
71. Benson DM Jr, Cohen AD, Jagannath S, Munshi NC, Spitzer G, Hofmeister CC, et al. A phase I trial of the anti-KIR antibody IPH2101 and lenalidomide in patients with relapsed/refractory multiple myeloma. Clin Cancer Res (2015) 21:4055-61. doi:10.1158/1078-0432.CCR-15-0304
72. Tarek N, Luduec J-L, Gallagher MM, Zheng J, Venstrom JM, Chamberlain E, et al. Unlicensed NK cells target neuroblastoma following anti-GD2 antibody treatment. J Clin Invest (2012) 122:3260-70. doi:10.1172/JCI62749
73. Leiden JM, Karpinski BA, Gottschalk L, Kornbluth J. Susceptibility to natural killer cell-mediated cytolysis is independent of the level of target cell class I HLA expression. J Immunol (1989) 142:2140-7
74. Nishimura MI, Stroynowski I, Hood L, Ostrand-Rosenberg S. H-2Kb antigen expression has no effect on natural killer susceptibility and tumorigenicity of a murine hepatoma. J Immunol (1988) 141:4403-9
75. Litwin V, Gumperz J, Parham P, Phillips JH, Lanier LL. Specificity of HLA class I antigen recognition by human NK clones: evidence for clonal heterogeneity, protection by self and non-self alleles, and influence of the target cell type. J Exp Med (1993) 178:1321-36. doi:10.1084/jem.178.4.1321
76. Guerra N, Tan YX, Joncker NT, Choy A, Gallardo F, Xiong N, et al. NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity (2008) 28:571-80. doi:10.1016/j.immuni.2008.02.016
77. Orange JS. Human natural killer cell deficiencies and susceptibility to infection. Microbes Infect (2002) 4:1545-58. doi:10.1016/S1286-4579(02)00038-2
78. 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) 131:1531-8
79. Kleijnen MF, Huppa JB, Lucin P, Mukherjee S, Farrell H, Campbell AE, et al. 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 (1997) 16:685-94. doi:10.1093/emboj/16.4.685
80. Krmpotic A, Messerle M, Crnkovic-Mertens I, Polic B, Jonjic S, Koszinowski UH. The immunoevasive function encoded by the mouse cytomegalovirus gene m152 protects the virus against T cell control in vivo. J Exp Med (1999) 190:1285-96. doi:10.1084/jem.190.9.1285
81. Reusch U, Muranyi W, Lucin P, Burgert HG, Hengel H, Koszinowski UH. A cytomegalovirus glycoprotein re-routes MHC class I complexes to lysosomes for degradation. EMBO J (1999) 18:1081-91. doi:10.1093/emboj/18.4.1081
82. Ziegler H, Thale R, Lucin P, Muranyi W, Flohr T, Hengel H, et al. A mouse cytomegalovirus glycoprotein retains MHC class I complexes in the ERGIC/cis-Golgi compartments. Immunity (1997) 6:57-66. doi:10.1016/S1074-7613(00)80242-3
83. Achdout H, Arnon TI, Markel G, Gonen-Gross T, Katz G, Lieberman N, et al. Enhanced recognition of human NK receptors after influenza virus infection. J Immunol (2003) 171:915-23. doi:10.4049/jimmunol.171.2.915
84. Achdout H, Manaster I, Mandelboim O. Influenza virus infection augments NK cell inhibition through reorganization of major histocompatibility complex class I proteins. J Virol (2008) 82:8030-7. doi:10.1128/JVI.00870-08
85. Wang B, Niu D, Lai L, Ren EC. p53 increases MHC class I expression by upregulating the endoplasmic reticulum aminopeptidase ERAP1. Nat Commun (2013) 4:2359. doi:10.1038/ncomms3359
86. Arase H, Mocarski ES, Campbell AE, Hill AB, Lanier LL. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science (2002) 296:1323-6. doi:10.1126/science.1070884
87. Smith HR, Heusel JW, Mehta IK, Kim S, Dorner BG, Naidenko OV, et al. Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc Natl Acad Sci U S A (2002) 99:8826-31. doi:10.1073/pnas.092258599
88. Tripathy SK, Smith HR, Holroyd EA, Pingel JT, Yokoyama WM. Expression of m157, a murine cytomegalovirus-encoded putative major histocompatibility class I (MHC-I)-like protein, is independent of viral regulation of host MHC-I. J Virol (2006) 80:545-50. doi:10.1128/JVI.80.1.545-550.2006
89. Revilleza MJ, Wang R, Mans J, Hong M, Natarajan K, Margulies DH. How the virus outsmarts the host: function and structure of cytomegalovirus MHC-I-like molecules in the evasion of natural killer cell surveillance. J Biomed Biotechnol (2011) 2011:724607. doi:10.1155/2011/724607
90. Shiroishi M, Tsumoto K, Amano K, Shirakihara Y, Colonna M, Braud VM, et al. Human inhibitory receptors Ig-like transcript 2 (ILT2) and ILT4 compete with CD8 for MHC class I binding and bind preferentially to HLA-G. Proc Natl Acad Sci U S A (2003) 100:8856-61. doi:10.1073/pnas.1431057100
91. Beck S, Barrell BG. Human cytomegalovirus encodes a glycoprotein homologous to MHC class-I antigens. Nature (1988) 331:269-72. doi:10.1038/331269a0
92. Prod'homme V, Griffin C, Aicheler RJ, Wang EC, McSharry BP, Rickards CR, et al. The human cytomegalovirus MHC class I homolog UL18 inhibits LIR-1+ but activates LIR-1-NK cells. J Immunol (2007) 178:4473-81. doi:10.4049/jimmunol.178.7.4473
93. Stewart CA, Laugier-Anfossi F, Vely F, Saulquin X, Riedmuller J, Tisserant A, et al. Recognition of peptide-MHC class I complexes by activating killer immunoglobulin-like receptors. Proc Natl Acad Sci U S A (2005) 102:13224-9. doi:10.1073/pnas.0503594102
94. Lee SH, Girard S, Macina D, Busa M, Zafer A, Belouchi A, et al. Susceptibility to mouse cytomegalovirus is associated with deletion of an activating natural killer cell receptor of the C-type lectin superfamily. Nat Genet (2001) 28:42-5. doi:10.1038/88247
95. 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) 186:1713-22. doi:10.4049/jimmunol.1003308
96. Forbes CA, Scalzo AA, Degli-Esposti MA, Coudert JD. Ly49C-dependent control of MCMV Infection by NK cells is cis-regulated by MHC class I molecules. PLoS Pathog (2014) 10:e1004161. doi:10.1371/journal.ppat.1004161
97. Kielczewska A, Pyzik M, Sun T, Krmpotic A, Lodoen MB, Munks MW, et al. Ly49P recognition of cytomegalovirus-infected cells expressing H2-Dk and CMV-encoded m04 correlates with the NK cell antiviral response. J Exp Med (2009) 206:515-23. doi:10.1084/jem.20080954
98. Xie X, Dighe A, Clark P, Sabastian P, Buss S, Brown MG. Deficient major histocompatibility complex-linked innate murine cytomegalovirus immunity in MA/My.L-H2b mice and viral downregulation of H-2k class I proteins. J Virol (2007) 81:229-36. doi:10.1128/JVI.00997-06
99. Brennan J, Lemieux S, Freeman JD, Mager DL, Takei F. Heterogeneity among Ly-49C natural killer (NK) cells: characterization of highly related receptors with differing functions and expression patterns. J Exp Med (1996) 184:2085-90. doi:10.1084/jem.184.6.2085
100. MacFarlane AW IV, Yamazaki T, Fang M, Sigal LJ, Kurosaki T, Campbell KS. Enhanced NK-cell development and function in BCAP-deficient mice. Blood (2008) 112:131-40. doi:10.1182/blood-2007-08-107847
101. Mahmoud AB, Tu MM, Wight A, Zein HS, Rahim MM, Lee SH, et al. Influenza virus targets class I MHC-educated NK cells for immunoevasion. PLoS Pathog (2016) 12:e1005446. doi:10.1371/journal.ppat.1005446
102. Sungur CM, Tang-Feldman YJ, Ames E, Alvarez M, Chen M, Longo DL, et al. Murine natural killer cell licensing and regulation by T regulatory cells in viral responses. Proc Natl Acad Sci U S A (2013) 110:7401-6. doi:10.1073/pnas.1218767110
103. Martin MP, Gao X, Lee JH, Nelson GW, Detels R, Goedert JJ, et al. Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nat Genet (2002) 31:429-34. doi:10.1038/ng934
104. Alter G, Martin MP, Teigen N, Carr WH, Suscovich TJ, Schneidewind A, et al. Differential natural killer cell-mediated inhibition of HIV-1 replication based on distinct KIR/HLA subtypes. J Exp Med (2007) 204:3027-36. doi:10.1084/jem.20070695
105. Alter G, Rihn S, Walter K, Nolting A, Martin M, Rosenberg ES, et al. HLA class I subtype-dependent expansion of KIR3DS1+ and KIR3DL1+ NK cells during acute human immunodeficiency virus type 1 infection. J Virol (2009) 83:6798-805. doi:10.1128/JVI.00256-09
106. Mavilio D, Lombardo G, Benjamin J, Kim D, Follman D, Marcenaro E, et al. Characterization of CD56-/CD16+ natural killer (NK) cells: a highly dysfunctional NK subset expanded in HIV-infected viremic individuals. Proc Natl Acad Sci U S A (2005) 102:2886-91. doi:10.1073/pnas.0409872102
107. de Rham C, Ferrari-Lacraz S, Jendly S, Schneiter G, Dayer JM, Villard J. The proinflammatory cytokines IL-2, IL-15 and IL-21 modulate the repertoire of mature human natural killer cell receptors. Arthritis Res Ther (2007) 9:R125. doi:10.1186/ar2336