Natural killer cell activation receptors in innate immunity to infection

Microbes and Infection

Volumn 4, Issue 15, 2002, Pages 1513-1521

  Yokoyama, Wayne M ^a   Scalzo, Anthony A ^b  

^a BARNES JEWISH HOSPITAL   (United States)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Cytomegalovirus; Innate immunity; NK cells

Indexed keywords

CD86 ANTIGEN; CELL RECEPTOR LY49H; CELL SURFACE RECEPTOR; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 12; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

CELL ACTIVATION; CELL PROLIFERATION; CELL SPECIFICITY; CYTOKINE PRODUCTION; CYTOLYSIS; DOWN REGULATION; HERPES VIRUS; HOST RESISTANCE; IMMUNITY; IN VIVO STUDY; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; VIRUS INFECTION; VIRUS RESISTANCE;

ANIMALS; IMMUNITY, NATURAL; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; RECEPTORS, IMMUNOLOGIC; VIRUS DISEASES;

CYTOMEGALOVIRUS;

EID: 0036927967     PISSN: 12864579     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1286-4579(02)00034-5     Document Type: Review

References (96)

1. Herberman R. NK Cells and Other Natural Effector Cells. 1982;Academic Press, New York, NY.
2. Bancroft G.J. The role of natural killer cells in innate resistance to infection. Curr. Opinion Immunol. 5:1993;503-510.
3. Biron C.A., Byron K.S., Sullivan J.L. Severe herpesvirus infections in an adolescent without natural killer cells. New England J. M. 320:1989;1731-1735.
4. Jawahar S., Moody C., Chan M., Finberg R., Geha R., Chatila T. Natural Killer (NK) cell deficiency associated with an epitope-deficient Fc receptor type IIIA (CD16-II). Clin. Exp. Immunol. 103:1996;408-413.
5. Biron C.A., Nguyen K.B., Pien G.C., Cousens L.P., Salazar-Mather T.P. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu. Rev. Immunol. 17:1999;189-220.
6. Shellam G.R., Allan J.E., Papadimitriou J.M., Bancroft G.J. Increased susceptibility to cytomegalovirus infection in beige mutant mice. Proc. Natl. Acad. Sci. USA. 78:1981;5104-5108.
7. Bukowski J.F., Woda B.A., Habu S., Okumura K., Welsh R.M. Natural killer cell depletion enhances virus synthesis and virus-induced hepatitis in vivo. J. Immunol. 131:1983;1531-1538.
8. Bukowski J.F., Woda B.A., Welsh R.M. Pathogenesis of murine cytomegalovirus infection in natural killer cell-depleted mice. J. Virol. 52:1984;119-128.
9. Welsh R.M., Dundon P.L., Eynon E.E., Brubaker J.O., Koo G.C., O'Donnell C.L. Demonstration of the antiviral role of natural killer cells in vivo with a natural killer cell-specific monoclonal antibody (NK 1.1). Nat. Immunity Cell Growth Regulation. 9:1990;112-120.
10. Orange J.S., Biron C.A. An absolute and restricted requirement for IL-12 in natural killer cell IFN-gamma production and antiviral defense. Studies of natural killer and T cell responses in contrasting viral infections. J. Immunol. 156:1996;1138-1142.
11. Henkart P.A. Lymphocyte-mediated cytotoxicity: two pathways and multiple effector molecules. Immunity. 1:1994;343-346.
12. Zamai L., Ahmad M., Bennett I.M., Azzoni L., Alnemri E.S., Perussia B. Natural killer (NK) cell-mediated cytotoxicity: differential use of TRAIL and Fas ligand by immature and mature primary human NK cells. J. Exp. M. 188:1998;2375-2380.
13. Bradley M., Zeytun A., Rafi-Janajreh A., Nagarkatti P.S., Nagarkatti M. Role of spontaneous and interleukin-2-induced natural killer cell activity in the cytotoxicity and rejection of Fas+ and Fas- tumor cells. Blood. 92:1998;4248-4255.
14. Karre K., Ljunggren H.G., Piontek G., Kiessling R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature. 319:1986;675-678.
15. Ljunggren H.G., Karre K. In search of the "missing self": MHC molecules and NK cell recognition. Immunol. Today. 11:1990;237-244.
16. Karre K. Herberman R.B., Callewaert D.M. Mechanisms of Cytotoxicity by NK Cells. DATE;81-92 Academic Press Inc, Orlando.
17. Karlhofer F.M., Ribaudo R.K., Yokoyama W.M. MHC class I alloantigen specificity of Ly-49+ IL-2-activated natural killer cells. Nature. 358:1992;66-70.
18. Yokoyama W.M. What goes up must come down: the emerging spectrum of inhibitory receptors. J. Exp. M. 186:1997;1803-1808.
19. Long E.O. Regulation of immune responses through inhibitory receptors. Annu. Rev. Immunol. 17:1999;875-904.
20. Yokoyama W.M. Natural killer cell receptors. Curr. Opinion Immunol. 7:1995;110-120.
21. Smith H.R.C., Karlhofer F.M., Yokoyama W.M. Ly-49 multigene family expressed by IL-2-activated NK cells. J. Immunol. 153:1994;1068-1079.
22. Biassoni R., Cantoni C., Falco M., Verdiani S., Bottino C., Vitale M., Conte R., Poggi A., Moretta A., Moretta L. The human leukocyte antigen (HLA)-C-specific "activatory" or "inhibitory" natural killer cell receptors display highly homologous extracellular domains but differ in their transmembrane and intracytoplasmic portions. J. Exp. M. 183:1996;645-650.
23. Mason L.H., Anderson S.K., Yokoyama W.M., Smith H.R.C., Winklerpickett R., Ortaldo J.R. The Ly-49D receptor activates murine natural killer cells. J. Exp. M. 184:1996;2119-2128.
24. Mason L.H., Willettebrown J., Anderson S.K., Gosselin P., Shores E.W., Love P.E., Ortaldo J.R., McVicar D.W. Characterization of an associated 16-KDa tyrosine phosphoprotein required for Ly-49D signal transduction. J. Immunol. 160:1998;4148-4152.
25. Tomasello E., Olcese L., Vely F., Geourgeon C., Blery M., Moqrich A., Gautheret D., Djabali M., Mattei M.G., Vivier E. Gene structure, expression pattern, and biological activity of mouse killer cell activating receptor-associated protein (KARAP)/DAP-12. J. Biol. Chem. 273:1998;34115-34119.
26. Chambers W.H., Vujanovic N.L., DeLeo A.B., Olszowy M.W., Herberman R.B., Hiserodt J.C. Monoclonal antibody to a triggering structure expressed on rat natural killer cells and adherent lymphokine-activated killer cells. J. Exp. M. 169:1989;1373-1389.
27. Lanier L.L., Corliss B., Wu J., Phillips J.H. Association of DAP12 with activating CD94/NKG2C NK cell receptors. Immunity. 8:1998;693-701.
28. Smith K.M., Wu J., Bakker A.B., Phillips J.H., Lanier L.L. Cutting edge: Ly-49D and Ly-49H associate with mouse DAP12 and form activating receptors. J. Immunol. 161:1998;7-10.
29. Bakker A.B., Hoek R.M., Cerwenka A., Blom B., Lucian L., McNeil T., Murray R., Phillips L.H., Sedgwick J.D., Lanier L.L. DAP12-deficient mice fail to develop autoimmunity due to impaired antigen priming. Immunity. 13:2000;345-353.
30. Lanier L.L., Cortiss B.C., Wu J., Leong C., Phillips J.H. Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature. 391:1998;703-707.
31. Anderson P., Caligiuri M., Ritz J., Schlossman S.F. CD3-negative natural killer cells express zeta TCR as part of a novel molecular complex. Nature. 341:1989;159-162.
32. Lanier L.L., Yu G., Phillips J.H. Co-association of CD3 zeta with a receptor (CD16) for IgG Fc on human natural killer cells. Nature. 342:1989;803-805.
33. + T cells. J. Exp. M. 186:1997;1957-1963.
34. Brumbaugh K.M., Binstadt B.A., Leibson P.J. Signal transduction during NK cell activation: balancing opposing forces. Curr. Topics Microbiol. Immunol. 230:1998;103-122.
35. Viver E., da Silva A.J., Ackerly M., Levine H., Rudd C.E., Anderson P. Association of a 70-kDa tyrosine phosphoprotein with the CD16: zeta: gamma complex expressed in human natural killer cells. Eur. J. Immunol. 23:1993;1872-1876.
36. Brumbaugh K.M., Binstadt B.A., Billadeau D.D., Schoon R.A., Dick C.J., Ten R.M., Leibson P.J. Functional role for syk tyrosine kinase in natural killer cell-mediated natural cytotoxicity. J. Exp. M. 186:1997;1965-1974.
37. Jevremovic D., Billadeau D.D., Schoon R.A., Dick C.J., Irvin B.J., Zhang W., Samelson L.E., Abraham R.T., Leibson P.J. Cutting edge: a role for the adaptor protein LAT in human NK cell-mediated cytotoxicity. J. Immunol. 162:1999;2453-2456.
38. Peterson E.J., Clements J.L., Ballas Z.K., Koretzky G.A. NK cytokine secretion and cytotoxicity occur independently of the SLP-76 adaptor protein. Eur. J. Immunol. 29:1999;2223-2232.
39. Jiang K., Zhong B., Gilvary D.L., Corliss B.C., Hong-Geller E., Wei S., Djeu J.Y. Pivotal role of phosphoinositide-3 kinase in regulation of cytotoxicity in natural killer cells. Nat. Immunol. 1:2000;419-425.
40. Wu J., Song Y., Bakker A.B., Bauer S., Spies T., Lanier L.L., Phillips J.H. An activating immunoreceptor complex formed by NKG2D and DAP10. Science. 285:1999;730-732. (see comments).
41. Wu J., Cherwinski H., Spies T., Phillips J.H., Lanier L.L. DAP10 and DAP12 form distinct, but functionally cooperative, receptor complexes in natural killer cells. J. Exp. M. 192:2000;1059-1068. (In Process Citation).
42. Groh V., Rhinehart R., Randolph-Habecker J., Topp M.S., Riddell S.R., Spies T. Costimulation of CD8alphabeta T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat. Immunol. 2:2001;255-260.
43. Yokoyama W.M. Now you see it, now you don't! Nat. Immunol. 1:2000;95-97.
44. Bauer S., Groh V., Wu J., Steinle A., Phillips J.H., Lanier L.L., Spies T. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science. 285:1999;727-729.
45. Diefenbach A., Jamieson A.M., Liu S.D., Shastri N., Raulet D.H. Novel ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nat. Immunol. 1:2000;119-126.
46. Cerwenka A., Bakker A.B.H., McClanahan T., Wagner J., Wu J., Phillips J.H., Lanier L.L. Retinoic acid early inducible genes define a ligand family for the activating NKG2D receptor in mice. Immunity. 12:2000;721-727.
47. Cosman D., Mullberg J., Sutherland C.L., Chin W., Armitage R., Fanslow W., Kubin M., Chalupny N.J. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity. 14:2001;123-133.
48. Idris A.H., Smith H.R.C., Mason L.H., Ortaldo J.H., Scalzo A.A., Yokoyama W.M. The natural killer cell complex genetic locus, Chok, encodes Ly49D, a target recognition receptor that activates natural killing. Proc. Natl. Acad. Sci. USA. 96:1999;6330-6335.
49. Nakamura M.C., Linnemeyer P.A., Niemi E.C., Mason L.H., Ortaldo J.R., Ryan J.C., Seaman W.E. Mouse Ly-49D recognizes H-2Dd and activates natural killer cell cytotoxicity. J. Exp. M. 189:1999;493-500.
50. George T.C., Mason L.H., Ortaldo J.R., Kumar V., Bennett M. Positive recognition of MHC class I molecules by the Ly49D receptor of murine NK cells. J. Immunol. 162:1999;2035-2043.
51. 2-microglobulin-deficient mice. J. Immmunol. 169:2002;126-136.
52. Karlhofer F.M., Ribaudo R.K., Yokoyama W.M. The interaction of Ly-49 with H-2Dd globally inactivates natural killer cell cytolytic activity. Trans. Assoc. Am. Physicians. 105:1992;72-85.
53. Correa I., Corral L., Raulet D.H. Multiple natural killer cell-activating signals are inhibited by major histocompatibility complex class I expression in target cells. Eur. J. Immunol. 24:1994;1323-1331.
54. Storkus W.J., Alexander J., Payne J.A., Dawson J.R., Cresswell P. Reversal of natural killing susceptibility in target cells expressing transfected class I HLA genes. Proc. Natl. Acad. Sci. USA. 86:1989;2361-2364.
55. Tortorella D., Gewurz B.E., Furman M.H., Schust D.J., Ploegh H.L. Viral subversion of the immune system. Annu. Rev. Immunol. 18:2000;861-926.
56. Cohen G.B., Gandhi R.T., Davis D.M., Mandelboim O., Chen B.K., Strominger J.L., Baltimore D. The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity. 10:1999;661-671.
57. Reyburn H.T., Mandelboim O., Vales-Gomez M., Davis D.M., Pazmany L., Strominger J.L. The class I MHC homologue of human cytomegalovirus inhibits attack by natural killer cells. Nature. 386:1997;514-517.
58. Farrell H.E., Vally H., Lynch D.M., Fleming P., Shellam G.R., Scalzo A.A., Davis-Poynter N.J. Inhibition of natural killer cells by a cytomegalovirus MHC class I homologue in vivo. Nature. 386:1997;510-514.
59. Cosman D., Fanger N., Borges L., Kubin M., Chin W., Peterson L., Hsu M.L. A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity. 7:1997;273-282.
60. Tomasec P., Braud V.M., Rickards C., Powell M.B., McSharry B.P., Gadola S., Cerundolo V., Borysiewicz L.K., McMichael A.J., Wilkinson G.W. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science. 287:2000;1031.
61. Ulbrecht M., Martinozzi S., Grzeschik M., Hengel H., Ellwart J.W., Pla M., Weiss E.H. Cutting edge: the human cytomegalovirus UL40 gene product contains a ligand for HLA-E and prevents NK cell-mediated lysis. J. Immunol. 164:2000;5019-5022.
62. Ishido S., Choi J.K., Lee B.S., Wang C., DeMaria M., Johnson R.P., Cohen G.B., Jung J.U. Inhibition of natural killer cell-mediated cytotoxicity by Kaposi's sarcoma-associated herpesvirus K5 protein. Immunity. 13:2000;365-374.
63. Cretney E., Degli-Esposti M.A., Densley E.H., Farrell H.E., Davis-Poynter N.J., Smyth M.J. m144, a murine cytomegalovirus (MCMV)-encoded major histocompatibility complex class I homologue, confers tumor resistance to natural killer cell-mediated rejection. J. Exp. M. 190:1999;435-444.
64. Ravetch J.V., Lanier L.L. Immune inhibitory receptors. Science. 290:2000;84-89.
65. Krmpotic A., Busch D.H., Bubic I.I., Gebhardt F., Hengel H., Hasan M., Scalzo A.A., Koszinowski U.H., Jonjic S. MCMV glycoprotein gp40 confers virus resistance to CD8(+) T cells and NK cells in vivo. Nat. Immunol. 2002.
66. Schmidt R.E., Bartley G., Levine H., Schlossman S.F., Ritz J. Functional characterization of LFA-1 antigens in the interaction of human NK clones and target cells. J. Immunol. 135:1985;1020-1025.
67. Mandelboim O., Lieberman N., Lev M., Paul L., Arnon T.I., Bushkin Y., Davis D.M., Strominger J.L., Yewdell J.W., Porgador A. Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature. 409:2001;1055-1060.
68. Arnon T.I., Lev M., Katz G., Chernobrov Y., Porgador A., Mandelboim O. Recognition of viral hemagglutinins by NKp44 but not by NKp30. Eur. J. Immunol. 31:2001;2680-2689.
69. Scalzo A.A., Fitzgerald N.A., Simmons A., La Vista A.B., Shellam G.R. Cmv-1, a genetic locus that controls murine cytomegalovirus replication in the spleen. J. Exp. M. 171:1990;1469-1483.
70. Scalzo A.A., Lyons P.A., Fitzgerald N.A., Forbes C.A., Yokoyama W.M., Shellam G.R. Genetic mapping of Cmv1 in the region of mouse chromosome 6 encoding the NK gene complex-associated loci Ly49 and musNKR-P1. Genomics. 27:1995;435-441.
71. Forbes C.A., Brown M.G., Cho R., Shellam G.R., Yokoyama W.M., Scalzo A.A. The Cmv1 host resistance locus is closely linked to the Ly49 multigene family within the natural killer cell gene complex on mouse chromosome 6. Genomics. 41:1997;406-413.
72. Depatie C., Muise E., Lepage P., Gros P., Vidal S.M. High-resolution linkage map in the proximity of the host resistance locus CMV1. Genomics. 39:1997;154-163.
73. Brown M.G., Scalzo A.A., Matsumoto K., Yokoyama W.M. The natural killer gene complex - a genetic basis for understanding natural killer cell function and innate immunity. Immunol. Rev. 155:1997;53-65.
74. Scalzo A.A., Fitzgerald N.A., Wallace C.R., Gibbons A.E., Smart Y.C., Burton R.C., Shellam G.R. The effect of the Cmv-1 resistance gene, which is linked to the natural killer cell gene complex, is mediated by natural killer cells. J. Immunol. 149:1992;581-589.
75. Brown M.G., Dokun A.O., Heusel J.W., Smith H.R., Beckman D.L., Blattenberger E.A., Dubbelde C.E., Stone L.R., Scalzo A.A., Yokoyama W.M. Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science. 292:2001;934-937.
76. Lee S.H., Girard S., Macina D., Busa M., Zafer A., Belouchi A., Gros P., Vidal S.M. Susceptibility to mouse cytomegalovirus is associated with deletion of an activating natural killer cell receptor of the C-type lectin superfamily. Nat. Genet. 28:2001;42-45.
77. 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. M. 194:2001;29-44.
78. Smith H.R., Chuang H.H., Wang L.L., Salcedo M., Heusel J.W., Yokoyama W.M. Nonstochastic coexpression of activation receptors on murine natural killer cells. J. Exp. M. 191:2000;1341-1354.
79. Sjolin H., Tomasello E., Mousavi-Jazi M., Bartolazzi A., Karre K., Vivier E., Cerboni C. Pivotal role of KARAP/DAP12 adaptor molecule in the natural killer cell-mediated resistance to murine cytomegalovirus infection. J. Exp. M. 195:2002;825-834.
80. Biron C.A., Turgiss L.R., Welsh R.M. Increase in NK cell number and turnover rate during acute viral infection. J. Immunol. 131:1983;1539-1545.
81. Biron C.A., Gazzinelli R.T. Effects of IL-12 on immune responses to microbial infections: a key mediator in regulating disease outcome. Curr. Opinion Immunol. 7:1995;485-496.
82. Dokun A.O., Kim S., Smith H.R., Kang H.S., Chu D.T., Yokoyama W.M. Specific and nonspecific NK cell activation during virus infection. Nat. Immunol. 2:2001;951-956.
83. 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.
84. 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., Scalzo A.A., Fremont D.H., Yokoyama W.M. Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc. Natl. Acad. Sci. USA. 99:2002;8826-8831.
85. Mehta I.K., Smith H.R.C., Wang J., Margulies D.H., Yokoyama W.M. A."chimeric" C57L-derived Ly49 inhibitory receptor resembling the Ly49D activation receptor. Cell Immunol. 209:2000;29-41.
86. Medzhitov R., Janeway C.A. Jr. Innate immune recognition and control of adaptive immune responses. Semin. Immunol. 10:1998;351-353.
87. Aderem A., Ulevitch R.J. Toll-like receptors in the induction of the innate immune response. Nature. 406:2000;782-787.
88. Hackett J. Jr, Bosma G.C., Bosma M.J., Bennett M., Kumar V. Transplantable progenitors of natural killer cells are distinct from those of T and B lymphocytes. Proc. Natl. Acad. Sci. USA. 83:1986;3427-3431.
89. Delano M.L., Brownstein D.G. Innate resistance to lethal mousepox is genetically linked to the NK gene complex on chromosome 6 and correlates with early restriction of virus replication by cells with an NK phenotype. J. Virol. 69:1995;5875-5877.
90. Pereira R.A., Scalzo A., Simmons A. Cutting edge: a NK complex-linked locus governs acute versus latent herpes simplex virus infection of neurons. J. Immunol. 166:2001;5869-5873.
91. Brownstein D.G., Bhatt P.N., Gras L., Jacoby R.O. Chromosomal locations and gonadal dependence of genes that mediate resistance to ectromelia (mousepox) virus-induced mortality. J. Virol. 65:1991;1946-1951.
92. Kim S., Iizuka K., Kang H.S., Dokun A., French A.R., Greco S., Yokoyama W.M. In vivo developmental stages in murine natural killer cell maturation. Nat. Immunol. 3:2002;523-528.
93. Kelley L.A., MacCallum R.M., Sternberg M.J. Enhanced genome annotation using structural profiles in the program 3D-PSSM. J. Mol. Biol. 299:2000;499-520.
94. Ziegler H., Thale R., Lucin P., Muranyi W., Flohr T., Hengel H., Farrell H., Rawlinson W., Koszinowski U.H. A mouse cytomegalovirus glycoprotein retains MHC class I complexes in the ERGIC/cis-Golgi compartments. Immunity. 6:1997;57-66.
95. Cuturi M.C., Anegon I., Sherman F., Loudon R., Clark S.C., Perussia B., Trinchieri G. Production of hematopoietic colony stimulating factors by human natural killer cells. J. Exp. M. 169:1989;569.
96. Kim S., Yokoyama W.M. NK cell granule exocytosis and cytokine production inhibited by Ly-49A engagement. Cell Immunol. 183:1998;106-112.