From sabotage to camouflage: Viral evasion of cytotoxic T lymphocyte and natural killer cell-mediated immunity

Seminars in Cell and Developmental Biology

Volumn 9, Issue 3, 1998, Pages 369-378

  Farrell, H E ^a,b   Davis Poynter, N J ^b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b ANIMAL HEALTH TRUST   (United Kingdom)

Author keywords

Cytotoxic T lymphocyte; Immune evasion; MHC class I; Natural killer cell; Virus

Indexed keywords

ANIMAL; BIOLOGICAL MODEL; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; HUMAN; IMMUNOLOGY; NATURAL KILLER CELL; REVIEW; VIRUS; VIRUS INFECTION;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; HUMANS; IMMUNITY, CELLULAR; KILLER CELLS, NATURAL; MODELS, IMMUNOLOGICAL; VIRUS DISEASES; VIRUSES;

EID: 0032092633     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1006/scdb.1998.0246     Document Type: Article

References (88)

1. Doherty PC, Allan W, Eichelberger M, Carding SR (1992) Roles of αβ and γδ T cell subsets in viral immunity. Annu Rev Immunol 10:123-151
2. Kagi D, Vignaux F, Lederman B, Burki K, Depraetere V, Nagata S, Hengartner H, Golstein P (1994) Fas perforin pathways as major mechanisms of cell-mediated cytotoxicity. Science 265:528-530
3. Lowing B, Hahne M, Mattmann C, Tschopp J (1994) Cytolytic T-cell cytotoxicity is mediated through perform and Fas lytic pathways. Nature 370:650-652
4. Guidotti LG, Ando K, Hobbs MV, Ishikawa T, Runkel L, Schreiber RD, Chisari FV (1994) Cytotoxic T lymphocytes inhibit hepatitis B virus gene expression by a non-cytolytic mechanism in transgenic mice. Proc Natl Acad Sci USA 91:3764-3768
5. Welsh RM, Tay CH, Varga SM, O'Donnell CL, Vergilis KL, Selin LK (1996) Lymphocyte-dependent 'natural' immunity to virus infections mediated by both natural killer cells and memory T cells. Semin Virol 7:95-102
6. Yap K, Ada G, McKenzie I (1978) Transfer of specific cytotoxic T lymphocytes protects mice inoculated with influenza virus. Nature 273:238-239
7. Kulkarni AB, Collins PL, Bacik I, Yewdell JW, Benink JR, Crowe JE, Murphy BR (1995) Cytotoxic T cells specific for a single peptide on the M2 protein of respiratory syncytial virus are the sole mediators of resistance induced by immunization with M2 encoded by a recombinant vaccinia virus. J Virol 69:1261-1264
8. Riddell SR, Watanabe KS, Goodrich JM, Li CR, Agha ME, Greenberg PD (1992) Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones. Science 257:238-241
9. Reddehase MJ, Mutter W, Munch K, Buhring HJ, Koszinowski UH (1987) CD8-positive T lymphocytes specific for murine cytomegalovirus immediate-early antigens mediate protective immunity J Virol 61:3102-3108
10. Bancroft GJ (1993) The role of natural killer cells in innate resistance to infection. Curr Opin Immunol 5:503-510
11. Biron CA (1997) Activation and function of natural killer cell responses during viral infections. Curr Opin Immunol 9:24-34.
12. Biron CA, Byron KS, Sullivan JL (1989) Severe herpesvirus infections in an adolescent without natural killer cells. N Engl J Med 320:1731-1735
13. Bonavida B, Katz J, Gottlieb M. (1986) Mechanism of defective NK cell activity in patients with acquired immunodeficiency syndrome (AIDS) and AIDS-related complex. J Immunol 137:1157-1163
14. Shellam GR, Allan JE, Papadimitriou JM, Bancroft GJ (1981) Increased susceptibility to cytomegalovirus infection in beige mutant mice. Proc Natl Acad Sci USA 78:5104-5108
15. Bukowski JF, Woda BA, Welsh RM (1984) Pathogenesis of murine cytomegalovirus infection in natural killer cell-depleted mice. J Virol 52:119-128
16. Bukowski JF, Warner JF, Dennert G, Welsh RM (1985) Adoptive transfer studies demonstrating the antiviral effects of natural killer cells in vivo. J Exp Med 161:40-52
17. Welsh RM, Brubaker JO, Vargas-Cortes M, O'Donnell CL. (1991). 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 virus infections occur independently of T and B cell functions. J Exp Med 173:1053-1063
18. + natural killer cells in C57BL/6 SCID mice infected with murine cytomegalovirus. Nat Immun 13:239-245
19. Tay CH, Welsh RM (1997) Distinct organ-dependent mechanisms for the control of murine cytomegalovirus infection by natural killer cells. J Virol 71:267-275
20. Scalzo AA, Lyons PA, Fitzgerald NA, Forbes CA, Yokoyama WM, Shellam GR (1995) Genetic mapping of Cmv1 in the region of mouse chromosome 6 encoding the NK gene complex-associated loci Ly49 and musNKR-P1. Genomics 27:435-441
21. DeLano ML Brownstein DG (1995) Innate resistance to lethal mousepox is linked to the NK gene complex on chromosome 6 and correlates with early restriction of virus by cells with an NK phenotype. J Virol 69:5875-5877
22. Bjorkman PJ, Saper MA, Samraoui B, Bennett WS, Strominger JL, Wiley DC (1987) Structure of the human class I histocompatibility antigen, HLA-A2. Nature 329:506-512
23. Rammensee H-G, Falk K, Rotzschke O (1993) Peptides naturally presented by MHC class I molecules. Annu Rev Immunol 11:213-244
24. Heemels MT, Ploegh HL (1995) Generation, translocation, and presentation of MHC class I-restricted peptides. Annu Rev Biochem 64:463-491
25. Brutkiewicz RR, Welsh RM (1995) Major histocompatibility complex class I antigens and the control of viral infections by natural killer cells. J Virol 69:3967-3971
26. Karre K (1995) Express yourself or die: peptides, MHC molecules, and NK cells. Science 267:978-979
27. Raulet DH (1996) Recognition events that inhibit and activate natural killer cells. Curr Opin Immunol 8:372-377
28. Kwong AD, Kruper JA, Frenkel N (1988) Herpes simplex virus virion host shutoff function. J Virol 62:912-921
29. Posavad CM, Newton JJ, Rosenthal K (1993) Inhibition of human CTL-mediated lysis by fibroblasts infected with herpes simplex virus. J Immunol 151:4865-4873
30. + CTL clones recognise HSV-2-infected fibroblasts after treatment with IFN-g or when virion host shutoff functions are disabled. J Immunol 156:3901-3910
31. Borysiewicz LK, Hickling JK, Graham S, Sinclair J, Cranage MP, Smith GL, Sissons JGP (1988) Human cytomegalovirus-specific cytotoxic T cells. Relative frequency of stage-specific CTL recognising the 72-kDa immediate early protein and glycoprotein B expressed by recombinant vaccinia viruses. J Exp Med 168:919-931
32. Gilbert MJ, Riddell SR, Plachter B, Greenberg PD (1996) Cytomegalovirus selectively blocks antigen processing and presentation of its immediate-early gene product. Nature 383:720-722
33. Levitskaya J, Coram M, Levitsky V, Imreh S, Steigerwald-Mullen PM, Klein G, Kurilla MG, Masucci MG (1995) Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1. Nature 375:685-688
34. York IA, Rock KL (1996) Antigen processing and presentation by the class I major histocompatibility complex. Annu Rev Immunol 14:369-396
35. Kelly A, Powis SH, Kerr L-A, Mockridge I, Elliot T, Bastin J, Uchanska-Ziegler B, Ziegler A, Trowsdale J, Townsend A (1992) Assembly and function of the two ABC transporter proteins encoded in the human major histocompatibility complex. Nature 355:641-644
36. + T cells. Cell 71:1205-1214
37. Früh K, Ahn K, Djaballah H, Sempe P, van Endert PM, Tampe R, Peterson PA, Yang Y (1995) A viral inhibitor of peptide transporters for antigen presentation. Nature 375:415-418
38. Hill A, Jugovic P, York I, Rus G, Bennink J, Yewdell J, Ploegh H, Johnson D (1995) Herpes simplex virus turns off the TAP to evade host immunity. Nature 375:411-415
39. + T lymphocytes. Cell 77:525-535
40. Ahn K, Meyer TH, Uebel S, Sempe P, Djaballah H, Yang Y, Peterson PA, Früh K, Tampe R (1996) Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus protein ICP47. EMBO J 15:3247-3255
41. Hill, AB, Barnett BC, McMichael AJ, McGeoch DJ (1994) HLA class I molecules are not transported to the cell surface in cells infected with herpes simplex virus types 1 and 2. J Immunol 152:2736-2741
42. Hengel H, Flohr T, Hammerlling GJ, Koszinowski UH, Momburg F (1996) Human Cytomegalovirus inhibits peptide translocation into the endoplasmic reticulum for MHC class I assembly. J Gen Virol 77:2287-2296
43. Ahn, K, Gruhler A, Galocha B, Jones TR, Wiertz EJHJ, Ploegh HL, Peterson PA, Yang Y, Früh K (1997) The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity 6:613-621
44. Hengel H, Koopman J-O, Flohr T, Muranyi W, Goulmy E, Hammerling GJ, Koszinowski UH, Momburg F (1997) A viral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter. Immunity 6:623-632
45. Rapoport TA, Jungnickel B, Kutay U (1996) Protein transport across the eukaryotic endoplasmic reticulum and bacterial inner membranes. Annu Rev Biochem 65:271-303
46. Wiertz EJHJ, Jones TR, Sun L, Bogyo M, Geuze HJ, Ploegh HL (1996) The human Cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84:769-779
47. Wiertz EJHJ, Tortorella D, Bogyo M, Yu J, Mothes W, Jones TR, Rapoport TA, Ploegh HL (1996) Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384:432-438
48. Plemper RK, Bohmler S, Bordallo J, Sommer T, Wolf DH (1997) Mutant analysis links the translocon and bip to retrograde protein transport for ER degradation. Nature 388:891-895
49. Machold RP, Wiertz EJHJ, Jones TR, Ploegh HL (1997) The HCMV gene products US11 and US2 differ in their ability to attack allelic forms of murine major histocompatibility complex (MHC) class I heavy chains. J Exp Med 185:363-366
50. Schwartz I, Marechal V, Le Gall S, Lemonnier F, Heard JM (1996) Endocytosis of major histocompatibilitycomplex class I molecules is induced by HIV-1 Nef protein. Nature Med 2:338-342
51. Mangasarian A, Foti M, Aiken C, Chin D, Carpentier JL, Trono D (1997) The HIV-1 Nef protein acts as a connector with sorting pathways in the Golgi and at the plasma membrane. Immunity 6:67-77
52. Kerkau T, Bacik I, Bennink JR, Yewdell JW, Hunig T, Schimpl A, Schubert U (1997) The human immunodeficiency virus type 1 (HIV-1) Vpu protein interferes with an early step in the biosynthesis of major histocompatibilitycomplex (MHC) class I molecules. J Exp Med 185:1295-1305
53. Willey R., Maldarelli F, Martin MA and Strebel K (1992) Human immunodeficiency virus type 1 Vpu protein induces rapid degradation of CD4. J Virol 66:7193-7200
54. Burget HG, Kvist S (1985) An adenovirus type 2 glycoprotein blocks cell surface expression of human histocompatibility class I antigens. Cell 41:987-997
55. Andersson M, Pääbo T, Nilsson T, Peterson PA (1985) Impaired intracellular transport of class I MHC antigen as a possible means for adenoviruses to evade immune surveillance. Cell 43:215-222
56. Horwitz MS, Tufariello J, Grunhaus A, Fejer G (1995) Model systems for studying the effects of adenovirus E3 genes on virulence in vivo. Curr Top Microbiol Immunol 199:195-211
57. Feuerbach D, Etteldorf S, Ebenau-Jehle C, Abastado JP, Madden D, Burgert H-G (1994) Identification of amino acids within the MHC molecule important for the interaction with the adenovirus protein E3/19K J Immunol 153:1626-1636
58. Gabathuler R, Levy F, Kvist S (1990) Requirements for the association of adenovirus type 2 E3/19K wild-type and mutant proteins with HLA antigens. J Virol 64:3679-3685
59. Pääbo S, Weber F, Nilsson T, Schaffner W, Peterson PA (1986) Structural and functional dissection of an MHC class I antigen-binding adenovirus glycoprotein. EMBO J 5:1921-1927
60. Hermiston TW, Tripp RA, Sparer T, Gooding LR, Wold WS (1993) Deletion mutation analysis of the adenovirus type 2 E3-19K protein: identification of sequences within the endoplasmic reticulum lumenal domain that are required for class I antigen binding and protection from adenovirus-specific cytotoxic T lymphocytes. J Virol 67:5289-5298
61. Beier DC, Cox JH, Vining DR, Cresswell P, Engelhard VH (1994) Association of human class I MHC alleles with the adenovirus E3/19K protein. J Immunol 152:3862-3872
62. Gabathuler R, Kvist S (1990) The endoplasmic reticulum retention signal of the E3/19K protein of adenovirus type 2 consists of three separate amino acid segments at the carboxy terminus. J Cell Biol 111:1803-1810
63. Jackson MR, Nilsson T, Peterson PA (1990) Identification of a consensus motif for retention of transmembrane proteins in the endoplasmic reticulum. EMBO J 9:3153-3162
64. Letourner F, Gaynor EC, Hennecke S, Demoliere C, Dude R, Emr S, Riezman H, Cosson P (1994) Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell 79:1199-1207
65. Rawle FC, Tollefson E, Wold WSM, Gooding LR (1989) Mouse anti-adenovirus T lymphocytes. Inhibition of lysis by E3 gp19K but not E3 14.7K. J Immunol 143:2031-2037
66. Grunhaus A, Cho S, Horwitz MS (1994) Association of vaccinia virus-expressed adenovirus E3 19K glycoprotein with class I MHC and its effects on virulence in a murine pneumonia model. Virology 200:535-546
67. Sparer TE, Tripp RA, Dillehay DL, Hermiston TW, Wold WSM, Gooding L (1996) The role of human adenovirus early region 3 proteins (gp19 K, 10.4 K, 14.5 K and 14.7 K) in a murine pneumonia model. J Virol 70:2431-2439
68. Ginsberg HS, Lundholm-Beauchamp U, Horswood RL, Pernis B, Wold WSM, Chanock RM, Prince GA (1989) Role of early region 3 (E3) in pathogenesis of adenovirus disease. Proc Natl Acad Sci USA 86:3823-3827
69. Ahn K, Angelo A, Ghazal P, Peterson PA, Yang Y, Früh K (1996) Human cytomegalovirus inhibits antigen presentation by a sequential multistep process. Proc Natl Acad Sci USA 93:10990-10995
70. Jones TR, Wiertz EJHJ, Sun L, Fish KN, Nelson JA, Ploegh HL (1996) Human cytomegalovirus US3 impairs transport and maturation of major histocompatibility complex class I heavy chains. Proc Natl Acad Sci USA 93:11327-11333
71. Thale R, Szepan U, Hengel H, Geginat G, Lucin P, Koszinowski UH (1995) Identification of the mouse cytomegalovirus genomic region affecting major histocompatibility complex class I molecule transport. J. Virol 69:6098-6105
72. Ziegler H, Thale R, Lucin P, Muranyi W, Flohr T, Hengel H, Farrell H, Rawlinson W, Koszinowski UH (1997) A mouse cytomegalovirus glycoprotein retains MHC class I complexes in the ERGIC/cis-Golgi compartments. Immunity 6:57-66
73. Kleinjen, MF, Huppa JB, Lucin P, Mukherjee S, Farrell H, Campbell AE, Koszinowski UH, Hill AB, Ploegh HL (1997) 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 16:685-694
74. York IA, Johnson DC (1993) Direct contact with Herpes simplex virus-infected cells results in inhibition of lymphokine-activated killer cells because of cell-to-cell spread of virus. J Infect Dis 168:1127-1132
75. Beck S, Barrell BG (1988) Human cytomegalovirus encodes a glycoprotein homologous to MHC class-I antigens. Nature 331:269-272
76. Rawlinson WD, Farrell HE, Barrell BG (1996) Analysis of the complete DNA sequence of murine cytomegalovirus. J Virol 70:8833-8849
77. Beisser PS, Bruggeman CA, Vink C. Unpublished data
78. Browne H, Smith G, Beck S, Minson T (1990) A complex between the MHC class I homologue encoded by human cytomegalovirus and β2 microglobulin. Nature 347:770-772
79. Fahnestock ML, Johnson JL, Feldman RMR, Neveu JM, Lane WS, Bjorkman PJ (1995) The MHC class I homolog encoded by human cytomegalovirus binds endogenous peptides. Immunity 3:583-590
80. Reyburn, HT, Mandelboim O, Vales-Gomez M, Davis DM, Pazmany L, Strominger JL (1997) The class I MHC homologue of human cytomegalovirus inhibits attack by natural killer cells. Nature 386:514-517
81. Cosman D, Fanger N, Borges L, Kubin M, Chin W, Peterson L, Hsu M-L (1997) A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 7:273-282
82. Farrell HE, Vally H, Lynch DM, Fleming P, Shellam GR, Scalzo AA, Davis-Poynter NJ (1997) Inhibition of natural killer cells by a cytomegalovirus MHC class I homologue in vivo. Nature 386:510-514
83. Chapman TL, Bjorkman PJ (1998) Characterization of a murine cytomegalovirus class I major histocompatibility complex (MHC) homolog: comparison to MHC molecules and to the human cytomegalovirus MHC homolog. J Virol 72:460-467
84. Senkevich TG, Bugert JJ, Sisler JR, Koonin EV, Darai G, Moss B (1996) Genome sequence of a human tumourigenic poxvirus: prediction of specific host response-evasion genes. Science 273:813-816
85. + T-cell responses are not inhibited by E3-19K in the presence of gamma interferon. J Virol 70:6314-6322
86. Hengel H, Eblinger C, Pool J, Goulmy E, Koszinowski UH (1995) Cytokines restore MHC class I complex formation and control antigen presentation in human cytomegalovirus-infected cells. J Gen Virol 76:2987-2997
87. Hengel H, Lucin P, Jonjic S, Ruppert T, Koszinowski UH (1994) Restoration of cytomegalovirus antigen presentation by gamma interferon combats viral escape. J Virol 68:289-297
88. Geginat G, Ruppert T, Hengel H, Holtappels R, Koszinowski UH (1997) IFN-gamma is a prerequisite for optimal antigen processing of viral peptides in vivo. J Immunol 158:3303-3310