Virus-driven evolution of natural killer cell receptors

Microbes and Infection

Volumn 4, Issue 15, 2002, Pages 1505-1512

  Arase, Hisashi ^a   Lanier, Lewis L ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cytomegalovirus; Major histocompatibility complex; NK cell

Indexed keywords

CELL RECEPTOR; CELL RECEPTOR LY49H; HLA C ANTIGEN; HLA E ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MESSENGER RNA; NATURAL KILLER CELL RECEPTOR P46; NEF PROTEIN; PROTEIN M144; PROTEIN UL16; PROTEIN UL18; PROTEIN US11; PROTEIN US2; PROTEIN US3; PROTEIN US6; UNCLASSIFIED DRUG; VIRUS PROTEIN;

CELLULAR IMMUNITY; CYTOMEGALOVIRUS; CYTOTOXIC T LYMPHOCYTE; DOWN REGULATION; EVOLUTION; HERPES VIRUS; HUMAN; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SEQUENCE HOMOLOGY; VIRUS IDENTIFICATION; VIRUS IMMUNITY; VIRUS INFECTION;

ANIMALS; ANTIGENS, LY; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; HUMANS; KILLER CELLS, NATURAL; LECTINS, C-TYPE; RECEPTORS, IMMUNOLOGIC; VIRUS DISEASES; VIRUSES;

CYTOMEGALOVIRUS;

EID: 0036932326     PISSN: 12864579     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1286-4579(02)00033-3     Document Type: Review

References (70)

1. 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.
2. 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.
3. 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.
4. 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.
5. Lee H.S., Gerard S., Macina D., Busa M., Zafer A., Belouchi A., Gros P., Vidal S.M. Susceptibility to mouse cytomegalovirus is associated with depletion of an activating natural killer cell receptor of the C-type lectin superfamily. Nat. Genet. 28:2001;42-45.
6. 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.
7. Biron C.A., Byron K.S., Sullivan J.L. Severe herpesvirus infections in an adolescent without natural killer cells. New Engl. J. M. 320:1989;1731-1735.
8. Sayos J., Wu C., Morra M., Wang N., Zhang X., Allen D., van Schaik S., Notarangelo L., Geha R., Roncarolo M.G., Oettgen H., De Vries J.E., Aversa G., Terhorst C. The X-linked lymphoproliferative-disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature. 395:1998;462-469.
9. Satterthwaite A.B., Rawlings D.J., Witte O.N. DSHP: A 'power bar' for sustained immune response? Proc. Natl. Acad. Sci. USA. 95:1998;13355-13357.
10. Nichols K.E., Harkin D.P., Levitz S., Krainer M., Kolquist K.A., Genovese C., Bernard A., Ferguson M., Zuo L., Snyder E. Inactivating mutations in an SH2 domain-encoding gene in X-linked lymphoproliferative syndrome. Proc. Natl. Acad. Sci. USA. 95:1998;13765-13770.
11. Tangye S.G., Phillips J.H., Lanier L.L., Nichols K.E. Cutting edge: functional requirement for SAP in 2B4-mediated activation of human natural killer cells as revealed by the X-linked lymphoproliferative syndrome. J. Immunol. 165:2000;2932-2936.
12. Bukowski J.F., Warner J.F., Dennert G., Welsh R.M. Adoptive transfer studies demonstrating the antiviral effect of natural killer cells in vivo. J. Exp. M. 161:1985;40-52.
13. Welsh R.M., Burbaker J.O., Vargas-Cortes M., O'Donnell C.L. Natural killer (NK) cell response to virus infections in mice with severe combined immunodeficiency. The stimulation of NK cells and the NK cell-dependent control of virus infections occur independently of T and B cell functions. J. Exp. M. 173:1991;1053-1063.
14. 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.
15. 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.
16. Smith K.M., Wu J., Bakker A.B.H., Phillips J.H., Lanier L.L. Ly49D and Ly49H associate with mouse DAP12 and form activating receptors. J. Immunol. 161:1998;7-10.
17. 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.
18. 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.
19. Pessino A., Sivori S., Bottino C., Malaspina A., Morelli L., Moretta L., Biassoni R., Moretta A. Molecular cloning of NKp46: a novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity. J. Exp. M. 188:1998;953-960.
20. 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.
21. Sivori S., Pende D., Bottino C., Marcenaro E., Pessino A., Biassoni R., Moretta L., Moretta A. 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. 29:1999;1656-1666.
22. Katz P., Yeager H. Jr, Whalen G., Evans M., Swartz R.P., Roecklein J. Natural killer cell-mediated lysis of Mycobacterium avium complex-infected monocytes. J. Clin. Immunol. 10:1990;71-77.
23. Klimpel G.R., Niesel D.W., Klimpel K.D. Natural cytotoxic effector cell activity against Shigella flexneri-infected HeLa cells. J. Immunol. 136:1986;1081-1086.
24. Bancroft G.J., Schreiber R.D., Bosma G.C., Bosma M.J., Unanue E.R. A T cell-independent mechanism of macrophage activation by interferon-γ J. Immunol. 139:1987;1104-1107.
25. Vankayalapati R., Wizel B., Weis S.E., Safi H., Lakey D.L., Mandelboim O., Samten B., Porgador A., Barnes P.F. The NKp46 receptor contributes to NK cell lysis of mononuclear phagocytes infected with an intracellular bacterium. J. Immunol. 168:2002;3451-3457.
26. 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.
27. Huard B., Fruh K. A role for MHC class I downregulation in NK cell lysis of herpes virus- infected cells. Eur. J. Immunol. 30:2000;509-515.
28. Fletcher J.M., Prentice H.G., Grundy J.E. Natural killer cell lysis of cytomegalovirus (CMV)-infected cells correlates with virally induced changes in cell surface lymphocyte function-associated antigen-3 (LFA-3) expression and not with the CMV-induced downregulation of cell surface class I HLA. J. Immunol. 161:1998;2365-2374.
29. Leong C.C., Chapman T.L., Bjorkman P.J., Formankova D., Mocarski E.S., Phillips J.H., Lanier L.L. Modulation of natural killer cell cytotoxicity in human cytomegalovirus infection: The role of endogenous class I MHC and a viral class I homolog. J. Exp. M. 187:1998;1681-1687.
30. Beck S., Barrell B.G. Human cytomegalovirus encodes a glycoprotein homologous to MHC class-I antigens. Nature. 331:1988;269-272.
31. Fahnestock M.L., Johnson J.L., Feldman R.M.R., Neveu J.M., Lane W.S., Bjorkman P.J. The MHC class I homolog encoded by human cytomegalovirus binds endogenous peptides. Immunity. 3:1995;583-590.
32. Farrell H.E., Vally Y., 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.
33. 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.
34. Cosman D., Fanger N., Borges L., Kibin 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.
35. 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.
36. Krmpotic A., Busch D.H., Bubic 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. 3:2002;529-535.
37. Kaye J., Browne H., Stoffel M., Minson T. The UL16 gene of human cytomegalovirus encodes a glycoprotein that is dispensable for growth in vitro. J. Virol. 66:1992;6609-6615.
38. Ishido S., Wang C., Lee B.S., Cohen G.B., Jung J.U. Downregulation of major histocompatibility complex class I molecules by Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins. J. Virol. 74:2000;5300-5309.
39. Coscoy L., Ganem D. Kaposi's sarcoma-associated herpesvirus encodes two proteins that block cell surface display of MHC class I chains by enhancing their endocytosis. Proc. Natl. Acad. Sci. USA. 97:2000;8051-8056.
40. Coscoy L., Ganem D. A viral protein that selectively downregulates ICAM-1 and B7-2 and modulates T cell costimulation. J. Clin. Invest. 107:2001;1599-1606.
41. 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.
42. 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 targets. J. Immunol. 135:1985;1020-1025.
43. 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.
44. Makrigiannis A.P., Pau A.T., Saleh A., Winkler-Pickett R., Ortaldo J.R., Anderson S.K., Class I. MHC-binding characteristics of the 129/J Ly49 repertoire. J. Immunol. 166:2001;5034-5043.
45. Mehta I.K., Smith H.R., Wang J., Margulies D.H., Yokoyama W.M. A "chimeric" c57l-derived ly49 inhibitory receptor resembling the ly49 d activation receptor. Cell Immunol. 209:2001;29-41.
46. Mason L.H., Anderson S.K., Yokoyama W.M., Smith H.R.C., Winkler-Pickett R., Ortaldo J.R. The Ly-49D receptor activates murine natural killer cells. J. Exp. M. 184:1996;2119-2128.
47. Nakamura M.C., Naper C., Niemi E.C., Spusta S.C., Rolstad B., Butcher G.W., Seaman W.E., Ryan J.C. Natural killing of xenogeneic cells mediated by the mouse Ly-49D receptor. J. Immunol. 163:1999;4694-4700.
48. Idris A.H., Smith H.R.C., Mason L.H., Ortaldo J.R., Scalzo A.A., Yokoyama W.M. The natural killer gene complex genetic locus Chok encodes Ly-49D, it target recognition receptor that activates natural killing. Proc. Natl. Acad. Sci. USA. 96:1999;6330-6335.
49. 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.
50. Ravetch J.V., Lanier L.L. Immune inhibitory receptors. Science. 290:2000;84-89.
51. Lanier L.L. Face off - the interplay between activating and inhibitory immune receptors. Curr. Opin. Immunol. 13:2001;326-331.
52. Vilches C., Parham P. KIR: diverse, rapidly evolving receptors of innate and adaptive immunity. Annu. Rev. Immunol. 20:2002;217-251.
53. Khakoo S.I., Rajalingam R., Shum B.P., Weidenbach K., Flodin L., Muir D.G., Canavez F., Cooper S.L., Valiante N.M., Lanier L.L., Parham P. Rapid evolution of NK cell receptor systems demonstrated by comparison of chimpanzees and humans. Immunity. 12:2000;687-698.
54. 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.
55. Braud V.M., Allan D.S.J., O'Callaghan C.A., Soderstrom K., D'Andrea A., Ogg G.S., Lazetic S., Young N.T., Bell J.I., Phillips J.H., Lanier L.L., McMichael A.J. HLA-E binds to natural killer cell receptors CD94/NKG2A, B, and C. Nature. 391:1998;795-798.
56. Valés-Gómez M., Reyburn H.T., Erskine R.A., Lopez-Botet M., Strominger J.L. 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. 18:1999;4250-4260.
57. Llano M., Lee N., Navarro F., Garcia P., Albar J.P., Geraghty D.E., Lopez-Botet M. HLA-E-bound peptides influence recognition by inhibitory and triggering CD94/NKG2 receptors: preferential response to an HLA-G-derived nanomer. Eur. J. Immunol. 28:1998;2854-2863.
58. Arase N., Arase H., Park S.Y., Ohno H., Ra C., Saito T. Association with FcRg is essential for activation signal through NKR-P1 (CD161) in natural killer (NK) cells and NK1.1+ T cells. J. Exp. M. 186:1997;1957-1963.
59. Carlyle J.R., Martin A., Mehra A., Attisano L., Tsui F.W., Zuniga-Pflucker J.C. Mouse NKR-P1B, a novel NK1.1 antigen with inhibitory function. J. Immunol. 162:1999;5917-5923.
60. Kubagawa H., Burrows P.D., Cooper M.D. A novel pair of immunoglobulin-like receptors expressed by B cells and myeloid cells. Proc. Natl. Acad. Sci. USA. 94:1997;5261-5266.
61. Maeda A., Kuorsaki M., Kurosaki T. Paired immunoglobulin-like receptor (PIR)-A is involved in activating mast cells through its association with Fc receptor γ chain. J. Exp. M. 188:1998;991-995.
62. Han X., Sterling H., Chen Y., Saginario C., Brown E.J., Frazier W.A., Lindberg F.P., Vignery A. CD47, a ligand for the macrophage fusion receptor, participates in macrophage multinucleation. J. Biol. Chem. 275:2000;37984-37992.
63. Vernon-Wilson E.F., Kee W.J., Willis A.C., Barclay A.N., Simmons D.L., Brown M.H. CD47 is a ligand for rat macrophage membrane signal regulatory protein SIRP (OX41) and human SIRPalpha 1. Eur. J. Immunol. 30:2000;2130-2137.
64. Oldenborg P.A., Zheleznyak A., Fang Y.F., Lagenaur C.F., Gresham H.D., Lindberg F.P. Role of CD47 as a marker of self on red blood cells. Science. 288:2000;2051-2054.
65. Tomasello E., Cant C., Buhring H.J., Vely F., Andre P., Seiffert M., Ullrich A., Vivier E. Association of signal-regulatory proteins beta with KARAP/DAP-12. Eur. J. Immunol. 30:2000;2147-2156.
66. Dietrich J., Cella M., Seiffert M., Buhring H.J., Colonna M. Cutting edge: signal-regulatory protein beta1 is a DAP12-associated activating receptor expressed in myeloid cells. J. Immunol. 164:2000;9-12.
67. Borges L., Hsu M.L., Fanger N., Kubin M., Cosman D. A family of human lymphoid and myeloid Ig-like receptors, some of which bind to MHC class I molecules. J. Immunol. 159:1997;5192-5196.
68. Colonna M., Navarro F., Bellon T., Llano M., Garcia P., Samaridi J., Angman L., Cella M., Lopez-Botet M. A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J. Exp. M. 186:1997;1809-1818.
69. Nakajima H., Samaridis J., Angman L., Colonna M. Human myeloid cells express an activating ILT receptor (ILT1) that associates with Fc receptor γ-chain. J. Immunol. 162:1999;5-8.
70. 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.