Activation of natural killer cells: Underlying molecular mechanisms revealed

Scandinavian Journal of Immunology

Volumn 60, Issue 1, 2004, Pages 14-22

  Backstrom E ^a,b   Kristensson, K ^a   Ljunggren, H G ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CD94 ANTIGEN; LIGAND; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL KILLER CELL RECEPTOR NKG2D;

CELL ACTIVATION; CELL FUNCTION; CELL INTERACTION; CELLULAR DISTRIBUTION; GENE LOCATION; HUMAN; IMMUNE RESPONSE; LYMPHOCYTE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TARGET CELL;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD94; ANTIGENS, LY; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; KILLER CELLS, NATURAL; LECTINS, C-TYPE; LIGANDS; LYMPHOCYTE ACTIVATION; MICE; RECEPTORS, IMMUNOLOGIC;

EID: 3242706106     PISSN: 03009475     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0300-9475.2004.01475.x     Document Type: Review

References (104)

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.
2. Kiessling R, Klein E, Pross H, Wigzell H. "Natural" killer cells in the mouse. II. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Characteristics of the killer cell. Eur J Immunol 1975;5:117-21.
3. Herberman RB, Nunn ME, Lavrin DH. Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic acid allogeneic tumors. I. Distribution of reactivity and specificity. Int J Cancer 1975;16:216-29.
4. Herberman RB, Nunn ME, Holden HT, Lavrin DH. Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic and allogeneic tumors. II. Characterization of effector cells. Int J Cancer 1975;16:230-9.
5. Scott P, Trinchieri G. The role of natural killer cells in host-parasite interactions. Curr Opin Immunol 1995;7:34-40.
6. Unanue ER. Inter-relationship among macrophages, natural killer cells and neutrophils in early stages of Listeria resistance. Curr Opin Immunol 1997;9:35-43.
7. Biron CA, Brossay L. NK cells and NKT cells in innate defense against viral infections. Curr Opin Immunol 2001;13:458-64.
8. Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol 1999;17:189-220.
9. Shi F, Ljunggren HG, Sarvetnick N. Innate immunity and autoimmunity: from self-protection to self-destruction. Trends Immunol 2001;22:97-101.
10. Raulet DH. Development and tolerance of natural killer cells. Curr Opin Immunol 1999;11:129-34.
11. +, Ly-49- cells from multipotential murine bone marrow progenitors in a stroma-free culture: definition of cytokine requirements and developmental intermediates. J Exp Med 1997;186:1609-14.
12. Colucci F, Caligiuri MA, Di Santo JP. What does it take to make a natural killer? Nat Rev Immunol 2003;3:413-25.
13. Ljunggren HG, Karre K. Host resistance directed selectively against H-2-deficient lymphoma variants. Analysis of the mechanism. J Exp Med 1985;162:1745-59.
14. Kärre 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.
15. Kärre K. NK cells, MHC class I molecules and the missing self. Scand J Immunol 2002;55:221-8.
16. Moretta L, Biassoni R, Bottino C, Mingari MC, Moretta A. Natural killer cells: a mystery no more. Scand J Immunol 2002;55:229-32.
17. Yokoyama WM. The search for the missing 'missing-self' receptor on natural killer cells. Scand J Immunol 2002;55:233-7.
18. Ljunggren HG, Kärre K. In search of the 'missing self': MHC molecules and NK cell recognition. Immunol Today 1990;11:237-44.
19. Lanier LL. On guard - activating NK cell receptors. Nat Immunol 2001;2:23-7.
20. Diefenbach A, Raulet DH. Innate immune recognition by stimulatory immunoreceptors. Curr Opin Immunol 2003;15:37-44.
21. Raulet DH. Roles of the NKG2D immunoreceptor and its ligands. Nat Rev Immunol 2003;3:781-90.
22. Diefenbach A, Jamieson AM, Liu SD, Shastri N, Raulet DH. Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nat Immunol 2000;1:119-26.
23. Cerwenka A, Bakker AB, McClanahan T et al. Retinoic acid early inducible genes define a ligand family for the activating NKG2D receptor in mice. Immunity 2000;12:721-7.
24. Cerwenka A, Lanier LL. Ligands for natural killer cell receptors: redundancy or specificity. Immunol Rev 2001;181:158-69.
25. Diefenbach A, Raulet DH. Strategies for target cell recognition by natural killer cells. Immunol Rev 2001;181:170-84.
26. Lanier LL. Face off - the interplay between activating and inhibitory immune receptors. Curr Opin Immunol 2001;13:326-31.
27. Davis DM. Assembly of the immunological synapse for T cells and NK cells. Trends Immunol 2002;23:356-63.
28. Monks CR, Freiberg BA, Kupfer H, Sciaky N, Kupfer A. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 1998;395:82-6.
29. Vyas YM, Maniar H, Dupont B. Cutting edge: differential segregation of the SRC homology 2-containing protein tyrosine phosphatase-1 within the early NK cell immune synapse distinguishes noncytolytic from cytolytic interactions. J Immunol 2002;168:3150-4.
30. Lanier LL. NK cell receptors. Annu Rev Immunol 1998;16:359-93.
31. Blery M, Olcese L, Vivier E. Early signaling via inhibitory and activating NK receptors. Hum Immunol 2000;61:51-64.
32. Lanier LL. Natural killer cell receptor signaling. Curr Opin Immunol 2003;15:308-14.
33. Stebbins CC, Watzl C, Billadeau DD, Leibson PJ, Burshtyn DN, Long EO. Vav1 dephosphorylation by the tyrosine phosphatase SHP-1 as a mechanism for inhibition of cellular cytotoxicity. Mol Cell Biol 2003;23:6291-9.
34. Billadeau DD, Brumbaugh KM, Dick CJ, Schoon RA, Bustelo XR, Leibson PJ. The Vav-Rac1 pathway in cytotoxic lymphocytes regulates the generation of cell-mediated killing. J Exp Med 1998;188:549-59.
35. Long EO, Barber DF, Burshtyn DN et al. Inhibition of natural killer cell activation signals by killer cell immunoglobulin-like receptors (CD158). Immunol Rev 2001;181:223-33.
36. Welch AY, Kasahara M, Spain LM. Identification of the mouse killer immunoglobulin-like receptor-like (Kirl) gene family mapping to Chromosome X. Immunogenetics 2003;54:782-90.
37. Hoelsbrekken SE, Nylenna O, Saether PC et al. Cutting edge: molecular cloning of a killer cell Ig-like receptor in the mouse and rat. J Immunol 2003;170:2259-63.
38. + IL-2-activated natural killer cells. Nature 1992;358:66-70.
39. Kane KP, Silver ET, Hazes B. Specificity and function of activating Ly-49 receptors. Immunol Rev 2001;181:104-14.
40. Anderson SK, Ortaldo JR, McVicar DW. The ever-expanding Ly49 gene family: repertoire and signaling. Immunol Rev 2001;181:79-89.
41. Lazetic S, Chang C, Houchins JP, Lanier LL, Phillips JH. Human natural killer cell receptors involved in MHC class I recognition are disulfide-linked heterodimers of CD94 and NKG2 subunits. J Immunol 1996;157:4741-5.
42. Plougastel B, Jones T, Trowsdale J. Genomic structure, chromosome location, and alternative splicing of the human NKG2A gene. Immunogenetics 1996;44:286-91.
43. Vance RE, Kraft JR, Altman JD, Jensen PE, Raulet DH. Mouse CD94/NKG2A is a natural killer cell receptor for the nonclassical major histocompatibility complex (MHC) class I molecule Qa-1(b). J Exp Med 1998;188:1841-8.
44. Braud VM, Allan DS, O'Callaghan CA et al. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 1998;391:795-9.
45. Colucci F, Di Santo JP, Leibson PJ. Natural killer cell activation in mice and men: different triggers for similar weapons? Nat Immunol 2002;3:807-13.
46. Wu J, Song Y, Bakker AB et al. An activating immunoreceptor complex formed by NKG2D and DAP10. Science 1999;285:730-2.
47. Billadeau DD, Upshaw JL, Schoon RA, Dick CJ, Leibson PJ. NKG2D-DAP10 triggers human NK cell-mediated killing via a Syk-independent regulatory pathway. Nat Immunol 2003;4:557-64.
48. Colucci F, Rosmaraki E, Bregenholt S et al. Functional dichotomy in natural killer cell signaling: Vav1-dependent and -independent mechanisms. J Exp Med 2001;193:1413-24.
49. Houchins JP, Yabe T, McSherry C, Bach FH. DNA sequence analysis of NKG2, a family of related cDNA clones encoding type II integral membrane proteins on human natural killer cells. J Exp Med 1991;173:1017-20.
50. Bauer S, Groh V, Wu J et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 1999;285:727-9.
51. Cosman D, Mullberg J, Sutherland CL et al. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 2001;14:123-33.
52. Carayannopoulos LN, Naidenko OV, Fremont DH, Yokoyama WM. Cutting edge: murine UL16-binding protein-like transcript 1: a newly described transcript encoding a high-affinity ligand for murine NKG2D. J Immunol 2002;169:4079-83.
53. Ho EL, Heusel JW, Brown MG, Matsumoto K, Scalzo AA, Yokoyama WM. Murine Nkg2d and Cd94 are clustered within the natural killer complex and are expressed independently in natural killer cells. Proc Natl Acad Sci USA 1998;95:6320-5.
54. Berg SF, Dissen E, Westgaard IH, Fossum S. Molecular characterization of rat NKR-P2, a lectin-like receptor expressed by NK cells and resting T cells. Int Immunol 1998;10:379-85.
55. Govaerts MM, Goddeeris BM. Homologues of natural killer cell receptors NKG2-D and NKR-P1 expressed in cattle. Vet Immunol Immunopathol 2001;80:339-44.
56. Yim D, Jie HB, Sotiriadis J et al. Molecular cloning and characterization of pig immunoreceptor DAP10 and NKG2D. Immunogenetics 2001;53:243-9.
57. LaBonte ML, Levy DB, Letvin NL. Characterization of rhesus monkey CD94/NKG2 family members and identification of novel transmembrane-deleted forms of NKG2-A, B, C, and D. Immunogenetics 2000;51:496-9.
58. Shum BP, Flodin LR, Muir DG et al. Conservation and variation in human and common chimpanzee CD94 and NKG2 genes. J Immunol 2002;168:240-52.
59. Diefenbach A, Tomasello E, Lucas M et al. Selective associations with signaling proteins determine stimulatory versus costimulatory activity of NKG2D. Nat Immunol 2002;3:1142-9.
60. Gilfillan S, Ho EL, Cella M, Yokoyama WM, Colonna M. NKG2D recruits two distinct adapters to trigger NK cell activation and costimulation. Nat Immunol 2002;3:1150-5.
61. Jamieson AM, Diefenbach A, McMahon CW, Xiong N, Carlyle JR, Raulet DH. The role of the NKG2D immunoreceptor in immune cell activation and natural killing. Immunity 2002;17:19-29.
62. Zompi S, Hamerman JA, Ogasawara K et al. NKG2D triggers cytotoxicity in mouse NK cells lacking DAP12 or Syk family kinases. Nat Immunol 2003;4:565-72.
63. Wu J, Cherwinski H, Spies T, Phillips JH, Lanier LL. DAP10 and DAP12 form distinct, but functionally cooperative, receptor complexes in natural killer cells. J Exp Med 2000;192:1059-68.
64. Yokoyama WM, Plougastel BF. Immune functions encoded by the natural killer gene complex. Nat Rev Immunol 2003;3:304-16.
65. Radaev S, Kattah M, Zou Z, Colonna M, Sun PD. Making sense of the diverse ligand recognition by NKG2D. J Immunol 2002;169:6279-85.
66. Groh V, Bahram S, Bauer S, Herman A, Beauchamp M, Spies T. Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc Natl Acad Sci USA 1996;93:12445-50.
67. Groh V, Rhinehart R, Secrist H, Bauer S, Grabstein KH, Spies T. Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proc Natl Acad Sci USA 1999;96:6879-84.
68. Weite SA, Sinzger C, Lutz SZ et al. Selective intracellular retention of virally induced NKG2D ligands by the human cytomegalovirus UL16 glycoprotein. Eur J Immunol 2003;33:194-203.
69. Groh V, Rhinehart R, Randolph-Habecker J, Topp MS, Riddell SR, Spies T. Costimulation of CD8alphabeta T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat Immunol 2001;2:255-60.
70. Das H, Groh V, Kuijl C et al. MICA engagement by human Vgamma2Vdelta2 T cells enhances their antigen-dependent effector function. Immunity 2001;15:83-93.
71. Tieng V, Le Bouguenec C, du Merle L et al. Binding of Escherichia coli adhesin AfaE to CD55 triggers cell-surface expression of the MHC class I-related molecule MICA. Proc Natl Acad Sci USA 2002;99:2977-82.
72. Jinushi M, Takehara T, Tatsumi T et al. Expression and role of MICA and MICB in human hepatocellular carcinomas and their regulation by retinoic acid. Int J Cancer 2003;104:354-61.
73. Kubin M, Cassiano L, Chalupny J et al. ULBP1, 2, 3: novel MHC class I-related molecules that bind to human cytomegalovirus glycoprotein UL16, activate NK cells. Eur J Immunol 2001;31:1428-37.
74. Jan Chalupny N, Sutherland CL, Lawrence WA, Rein-Weston A, Cosman D. ULBP4 is a novel ligand for human NKG2D. Biochem Biophys Res Commun 2003;305:129-35.
75. Nomura M, Takihara Y, Shimada K. Isolation and characterization of retinoic acid-inducible cDNA clones in F9 cells: one of the early inducible clones encodes a novel protein sharing several highly homologous regions with a Drosophila polyhomeotic protein. Differentiation 1994;57:39-50.
76. Malarkannan S, Shih PP, Eden PA et al. The molecular and functional characterization of a dominant minor H antigen, H60. J Immunol 1998;161:3501-9.
77. Zou Z, Nomura M, Takihara Y, Yasunaga T, Shimada K. Isolation and characterization of retinoic acid-inducible cDNA clones in F9 cells: a novel cDNA family encodes cell surface proteins sharing partial homology with MHC class I molecules. J Biochem (Tokyo) 1996;119:319-28.
78. Nomura M, Zou Z, Joh T, Takihara Y, Matsuda Y, Shimada K. Genomic structures and characterization of Rae1 family members encoding GPI-anchored cell surface proteins and expressed predominantly in embryonic mouse brain. J Biochem (Tokyo) 1996;120:987-95.
79. Cerwenka A, Baron JL, Lanier LL. Ectopic expression of retinoic acid early inducible-1 gene (RAE-1) permits natural killer cell-mediated rejection of a MHC class I-bearing tumor in vivo. Proc Natl Acad Sci USA 2001;98:11521-6.
80. Diefenbach A, Jensen ER, Jamieson AM, Raulet DH. Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 2001;413:165-71.
81. Hayakawa Y, Kelly JM, Westwood JA et al. Cutting edge: tumor rejection mediated by NKG2D receptor-ligand interaction is dependent upon perforin. J Immunol 2002;169:5377-81.
82. Backström E, Chambers BJ, Kristensson K, Ljunggren HG. Direct NK cell-mediated lysis of syngenic dorsal root ganglia neurons in vitro. J Immunol 2000;165:4895-900.
83. Backström E, Chambers BJ, Ho EL et al. Natural killer cell-mediated lysis of dorsal toot ganglia neurons via RAE1/NKG2D interactions. Eur J Immunol 2003;33:92-100.
84. Lodoen M, Ogasawara K, Hamerman JA et al. NKG2D-mediated natural killer cell protection against cytomegalovirus is impaired by viral gp40 modulation of retinoic acid early inducible 1 gene molecules. J Exp Med 2003;197:1245-53.
85. Diefenbach A, Hsia JK, Hsiung MY, Raulet DH. A novel ligand for the NKG2D receptor activates NK cells and macrophages and induces tumor immunity. Eur J Immunol 2003;33:381-91.
86. Kasahara M, Watanabe Y, Sumasu M, Nagata T. A family of MHC class I-like genes located in the vicinity of the mouse leukocyte receptor complex. Proc Natl Acad Sci USA 2002;99:13687-92.
87. Lanier LL, Corliss BC, Wu J, Leong C, Phillips JH. Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature 1998;391:703-7.
88. Bakker AB, Hoek RM, Cerwenka A et al. DAP12-deficient mice fail to develop autoimmunity due to impaired antigen priming. Immunity 2000;13:345-53.
89. Sjölin H, Tomasello E, Mousavi-Jazi M et al. Pivotal role of KARAP/DAP12 adaptor molecule in the natural killer cell-mediated resistance to murine cytomegalovirus infection. J Exp Med 2002;195:825-34.
90. Smith HR, Heusel JW, Mehta IK et al. Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc Natl Acad Sci USA 2002;99:8826-31.
91. Lee SH, Girard S, Macina D 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.
92. Brown MG, Dokun AO, Heusel JW et al. Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science 2001;292:934-7.
93. 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.
94. Houchins JP, Lanier LL, Niemi EC, Phillips JH, Ryan JC. Natural killer cell cytolytic activity is inhibited by NKG2-A and activated by NKG2-C. J Immunol 1997;158:3603-9.
95. Vales-Gomez M, Reyburn HT, Erskine RA, Lopez-Botet M, Strominger JL. Kinetics and peptide dependency of the binding of the inhibitory NK receptor CD94/NKG2-A and the activating receptor CD94/NKG2-C to HLA-E. EMBO J 1999;18:4250-60.
96. Michaëlsson J, de Matos CT, Achour A, Lanier LL, Kärre K, Söderström K. A signal peptide derived from hsp60 binds HLA-E and interferes with CD94/NKG2A recognition. J Exp Med 2002;196:1403-14.
97. Kraft JR, Vance RE, Pohl J, Martin AM, Raulet DH, Jensen PE. Analysis of Qa-1(b) peptide binding specificity and the capacity of CD94/NKG2A to discriminate between Qa-1-peptide complexes. J Exp Med 2000;192:613-24.
98. Moretta A, Bottino C, Vitale M et al. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol 2001;19:197-223.
99. Sivori S, Pende D, Bottino C et al. NKp46 is the major triggering receptor involved in the natural cytotoxicity of fresh or cultured human NK cells. Correlation between surface density of NKp46 and natural cytotoxicity against autologous, allogeneic or xenogeneic target cells. Eur J Immunol 1999;29:1656-66.
100. Mandelboim O, Lieberman N, Lev M et al. Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 2001;409:1055-60.
101. Arnon TI, Lev M, Katz G, Chernobrov Y, Porgador A, Mandelboim O, Recognition of viral hemagglutinins by NKp44 but not by NKp30. Eur J Immunol 2001;31:2680-9.
102. Pessino A, Sivori S, Bottino C et al. Molecular cloning of NKp46: a novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity. J Exp Med 1998;188:953-60.
103. Biassoni R, Pessino A, Bottino C, Pende D, Moretta L, Moretta A. The murine homologue of the human NKp46, a triggering receptor involved in the induction of natural cytotoxicity. Eur J Immunol 1999;29:1014-20.
104. Tangye SG, Phillips JH, Lanier LL. The CD2-subset of the Ig superfamily of cell surface molecules: receptor-ligand pairs expressed by NK cells and other immune cells. Semin Immunol 2000;12:149-57.