Coordinated function of murine cytomegalovirus genes completely inhibits CTL lysis

Journal of Immunology

Volumn 177, Issue 5, 2006, Pages 3225-3234

  Pinto, Amelia K ^a   Munks, Michael W ^a   Koszinowski, Ulrich H ^b   Hill, Ann B ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; CELL SPECIFICITY; CONTROLLED STUDY; CYTOLYSIS; CYTOMEGALOVIRUS; CYTOTOXIC T LYMPHOCYTE; EPITOPE MAPPING; FEMALE; INHIBITION KINETICS; M04 GENE; M06 GENE; M152 GENE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; VIPR GENE; VIRUS GENE; VIRUS MUTANT; VIRUS REPLICATION;

EID: 33747803947     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.5.3225     Document Type: Article

References (73)

1. Yewdell, J. W., and A. B. Hill. 2002. Viral interference with antigen presentation. Nat. Immunol. 3: 1019-1025.
2. del Val, M., H. Hengel, H. Hacker, U. Hartlaub, T. Ruppert, P. Lucin, and U. H. Koszinowski. 1992. Cytomegalovirus prevents antigen presentation by blocking the transport of peptide-loaded major histocompatibility complex class I molecules into the medial-Golgi compartment. J. Exp. Med. 176: 729-738.
3. Thale, R., U. Szepan, H. Hengel, G. Geginat, P. Lucin, and U. H. Koszinowski. 1995. Identification of the mouse cytomegalovirus genomic region affecting major histocompatibility complex class I molecule transport. J. Virol. 69: 6098-6105.
4. Ziegler, H., R. Thale, P. Lucin, W. Muranyi, T. Flohr, H. Hengel, H. Farrell, W. Rawlinson, and U. H. Koszinowski. 1997. A mouse cytomegalovirus glycoprotein retains MHC class I complexes in the ERGIC/cis-Golgi compartments. Immunity 6: 57-66.
5. Reusch, U., W. Muranyi, P. Lucin, H. G. Burgert, H. Hengel, and U. H. Koszinowski. 1999. A cytomegalovirus glycoprotein re-routes MHC class I complexes to lysosomes for degradation. EMBO J. 18: 1081-1091.
6. Wagner, M., A. Gutermann, J. Podlech, M. J. Reddehase, and U. H. Koszinowski. 2002. Major histocompatibility complex class I allele-specific cooperative and competitive interactions between immune evasion proteins of cytomegalovirus. J. Exp. Med. 196: 805-816.
7. Hengel, H., U. Reusch, A. Gutermann, H. Ziegler, S. Jonjic, P. Lucin, and U. H. Koszinowski. 1999. Cytomegaloviral control of MHC class I function in the mouse. Immunol. Rev. 168: 167-176.
8. Kleijnen, M. F., J. B. Huppa, P. Lucin, S. Mukherjee, H. Farrell, A. E. Campbell, U. H. Koszinowski, A. B. Hill, and H. L. Ploegh. 1997. A mouse cytomegalovirus glycoprotein, gp34, forms a complex with folded class 1 MHC molecules in the ER which is not retained but is transported to the cell surface. EMBO J. 16: 685-694.
9. Kavanagh, D. G., U. H. Koszinowski, and A. B. Hill. 2001. The murine cytomegalovirus immune evasion protein m4/gp34 forms biochemically distinct complexes with class I MHC at the cell surface and in a pre-Golgi compartment. J. Immunol. 167: 3894-3902.
10. Kavanagh, D. G., M. C. Gold, M. Wagner, U. H. Koszinowski, and A. B. Hill. 2001. The multiple immune-evasion genes of murine cytomegalovirus are not redundant: m4 and m152 inhibit antigen presentation in a complementary and cooperative fashion. J. Exp. Med. 194: 967-978.
11. b-restricted antigen presentation in primary macrophages by murine cytomegalovirus. J. Virol. 77: 301-308.
12. Krogsgaard, M., J. B. Huppa, M. A. Purbhoo, and M. M. Davis. 2003. Linking molecular and cellular events in T-cell activation and synapse formation. Semin. Immunol. 15: 307-315.
13. Munks, M. W., M. C. Gold, A. L. Zajac, C. M. Doom, C. S. Morello, D. H. Spector, and A. B. Hill. 2006. Genome-wide analysis reveals a highly diverse CD8 T cell response to murine cytomegalovirus. J. Immunol. 176: 3760-3766.
14. Cavanaugh, V. J., R. M. Stenberg, T. L. Staley, H. W. Virgin 4th, M. R. MacDonald, S. Paetzold, H. E. Farrell, W. D. Rawlinson, and A. E. Campbell. 1996. Murine cytomegalovirus with a deletion of genes spanning HindIII-J and -I displays altered cell and tissue tropism. J. Virol. 70: 1365-1374.
15. Driessen, C., R. A. Bryant, A. M. Lennon-Dumenil, J. A. Villadangos, P. W. Bryant, G. P. Shi, H. A. Chapman, and H. L. Ploegh. 1999. Cathepsin S controls the trafficking and maturation of MHC class II molecules in dendritic cells. J. Cell Biol. 147: 775-790.
16. Bouwer, H. G., M. S. Seaman, J. Forman, and D. J. Hinrichs. 1997. MHC class 1b-restricted cells contribute to antilisterial immunity: evidence for Qa-1b as a key restricting element for Listeria-specific CTLs. J. Immunol. 159: 2795-2801.
17. Wagner, M., S. Jonjic, U. H. Koszinowski, and M. Messerle. 1999. Systematic excision of vector sequences from the BAC-cloned herpesvirus genome during virus reconstitution. J. Virol. 73: 7056-7060.
18. Brune, W., Hengel Hartmut, Koszinowski Ulrich H. 2006. A mouse model for cytomegalovirus infection. In Current Protocols in Immunology. John Wiley and Sons, New York.
19. Loh, L. C., N. Balachandran, and L. F. Qualtiere. 1988. Characterization of a major virion envelope glycoprotein complex of murine cytomegalovirus and its immunological cross-reactivity with human cytomegalovirus. Virology 166: 206-216.
20. Loh, L. C., and L. F. Qualtiere. 1988. A neutralizing monoclonal antibody recognizes an 87K envelope glycoprotein on the murine cytomegalovirus virion. Virology 162: 498-502.
21. Rapp, M., P. Lucin, M. Messerle, L. C. Loh, and U. H. Koszinowski. 1994. Expression of the murine cytomegalovirus glycoprotein H by recombinant vaccinia virus. J. Gen. Virol. 75: 183-188 (Pt 1).
22. Del Val, M., H. Volkmer, J. B. Rothbard, S. Jonjic, M. Messerle, J. Schickedanz, M. J. Reddehase, and U. H. Koszinowski. 1988. Molecular basis for cytolytic T-lymphocyte recognition of the murine cytomegalovirus immediate-early protein pp89. J. Virol. 62: 3965-3972.
23. Hardy, R. 1986. Purification and coupling of fluorescent proteins for use in flow cytometry. In Handbook of Experimental Immunology, 4th Ed. D. M. Weir, L. A. Herzenberg, and C. Blackwell, eds. Blackwell Scientific Publications, Boston, pp. 31.1-31.12.
24. Pollock, J. L., R. M. Presti, S. Paetzold, and H. W. Virgin 4th. 1997. Latent murine cytomegalovirus infection in macrophages. Virology 227: 168-179.
25. Reddehase, M. J., W. Mutter, K. Munch, H. J. Buhring, and U. H. Koszinowski. 1987. CD8-positive T lymphocytes specific for murine cytomegalovirus immediate-early antigens mediate protective immunity. J. Virol. 61: 3102-3108.
26. Terhune, S. S., J. Schroer, and T. Shenk. 2004. RNAs are packaged into human cytomegalovirus virions in proportion to their intracellular concentration. J. Virol. 78: 10390-10398.
27. Sciortino, M.-T., M. Suzuki, B. Taddeo, and B. Roizman. 2001. RNAs extracted from herpes simplex virus 1 virions: apparent selectivity of viral but not cellular RNAs packaged in virions. J. Virol. 75: 8105-8116.
28. Bresnahan, W. A., and T. Shenk. 2000. A subset of viral transcripts packaged within human cytomegalovirus particles. Science 288: 2373-2376.
29. Holtappels, R., N. K. Grzimek, C. O. Simon, D. Thomas, D. Dreis, and M. J. Reddehase. 2002. Processing and presentation of murine cytomegalovirus pORFm164-derived peptide in fibroblasts in the face of all viral immunosubversive early gene functions. J. Virol. 76: 6044-6053.
30. Gold, M. C., M. W. Munks, M. Wagner, C. W. McMahon, A. Kelly, D. G. Kavanagh, M. K. Slifka, U. H. Koszinowski, D. H. Raulet, and A. B. Hill. 2004. Murine cytomegalovirus interference with antigen presentation has little effect on the size or the effector memory phenotype of the CD8 T cell response. J. Immunol. 172: 6944-6953.
31. Holtappels, R., J. Podlech, M.-F. Pahl-Seibert, M. Julch, D. Thomas, C. O. Simon, M. Wagner, and M. J. Reddehase. 2004. Cytomegalovirus misleads its host by priming of CD8 T cells specific for an epitope not presented in infected tissues. J. Exp. Med. 199: 131-136.
32. Lu, X., A. K. Pinto, A. M. Kelly, K. S. Cho, and A. B. Hill. 2006. Murine cytomegalovirus interference with antigen presentation contributes to the inability of CD8 T cells to control virus in the salivary gland. J. Virol. 80: 4200-4202.
33. Machold, R. P., E. J. Wiertz, T. R. Jones, and H. L. Ploegh. 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.
34. Wiertz, E. J., T. R. Jones, L. Sun, M. Bogyo, H. J. Geuze, and H. L. Ploegh. 1996. The human cytomegalovirus USl I gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84: 769-779.
35. Stevenson, P. G., S. Efstathiou, P. C. Doherty, and P. J. Lehner. 2000. Inhibition of MHC class I-restricted antigen presentation by γ2-herpesviruses. Proc. Natl. Acad. Sci. USA 97: 8455-8460.
36. Ishido, S., C. Wang, B.-S. Lee, G. B. Cohen, and J. U. Jung. 2000. Downregulation of major histocompatibility complex class I molecules by Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins. J. Virol. 74: 5300-5309.
37. Coscoy, L., and D. Ganem. 2000. 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: 8051-8056.
38. Loenen, W. A. M., C. A. Bruggeman, and E. J. H. J. Wiertz. 2001. Immune evasion by human cytomegalovirus: lessons in immunology and cell biology. Semin. Immunol. 13: 41-49.
39. Ahn, K., A. Angulo, P. Ghazal, P. A. Peterson, Y. Yang, and K. Fruh. 1996. Human cytomegalovirus inhibits antigen presentation by a sequential multistep process. Proc. Natl. Acad. Sci. USA 93: 10990-10995.
40. Kattenhorn, L. M., R. Mills, M. Wagner, A. Lomsadze, V. Makeev, M. Borodovsky, H. L. Ploegh, and B. M. Kessler. 2004. Identification of proteins associated with murine cytomegalovirus virions. J. Virol. 78: 11187-11197.
41. Rawlinson, W. D., H. E. Farrell, and B. G. Barrell. 1996. Analysis of the complete DNA sequence of murine cytomegalovirus. J. Virol. 70: 8833-8849.
42. Davis-Poynter, N. J., D. M. Lynch, H. Vally, G. R. Shellam, W. D. Rawlinson, B. G. Barrell, and H. E. Farrell. 1997. Identification and characterization of a G protein-coupled receptor homolog encoded by murine cytomegalovirus. J. Virol. 71: 1521-1529.
43. Melnychuk, R. M., P. Smith, C. N. Kreklywich, F. Ruchti, J. Vomaske, L. Hall, L. Loh, J. A. Nelson, S. L. Orloff, and D. N. Streblow. 2005. Mouse cytomegalovirus M33 is necessary and sufficient in virus-induced vascular smooth muscle cell migration. J. Virol. 79: 10788-10795.
44. McCormick, A. L., A. Skaletskaya, P. A. Barry, E. S. Mocarski, and V. S. Goldmacher. 2003. Differential function and expression of the viral inhibitor of caspase 8-induced apoptosis (vICA) and the viral mitochondria-localized inhibitor of apoptosis (vMIA) cell death suppressors conserved in primate and rodent cytomegaloviruses. Virology 316: 221-233.
45. Menard, C., M. Wagner, Z. Ruzsics, K. Holak, W. Brune, A. E. Campbell, and U. H. Koszinowski. 2003. Role of murine cytomegalovirus US22 gene family members in replication in macrophages. J. Virol. 77: 5557-5570.
46. McCormick, A. L., C. D. Meiering, G. B. Smith, and E. S. Mocarski. 2005. Mitochondrial cell death suppressors carried by human and murine cytomegalovirus confer resistance to proteasome inhibitor-induced apoptosis. J. Virol. 79: 12205-12217.
47. Loh, L. C., V. D. Keeler, and J. D. Shanley. 1999. Sequence requirements for the nuclear localization of the murine cytomegalovirus M44 gene product pp50. Virology 259: 43-59.
48. Loh, L. C., D. Locke, R. Melnychuk, and S. Laferte. 2000. The RGD sequence in the cytomegalovirus DNA polymerase accessory protein can mediate cell adhesion. Virology 272: 302-314.
49. Brune, W., C. Menard, J. Heesemann, and U. H. Koszinowski. 2001. A ribonucleotide reductase homolog of cytomegalovirus and endothelial cell tropism. Science 291: 303-305.
50. Gold, M. C., M. W. Munks, M. Wagner, U. H. Koszinowski, A. B. Hill, and S. P. Fling. 2002. The murine cytomegalovirus immunomodulatory gene m152 prevents recognition of infected cells by M45-specific CTL but does not alter the immunodominance of the M45-specific CD8 T cell response in vivo. J. Immunol. 169: 359-365.
51. Lembo, D., G. Gribaudo, A. Hofer, L. Riera, M. Cornaglia, A. Mondo, A. Angeretti, M. Gariglio, L. Thelander, and S. Landolfo. 2000. Expression of an altered ribonucleotide reductase activity associated with the replication of murine cytomegalovirus in quiescent fibroblasts. J. Virol. 74: 11557-11565.
52. Messerle, M., G. M. Keil, K. Schneider, and U. H. Koszinowski. 1992. Characterization of the murine cytomegalovirus genes encoding the major DNA binding protein and the ICP18.5 homolog. Virology 191: 355-367.
53. Oliveira, S. A., and T. E. Shenk. 2001. Murine cytomegalovirus M78 protein, a G protein-coupled receptor homologue, is a constituent of the virion and facilitates accumulation of immediate-early viral mRNA. Proc. Natl. Acad. Sci. USA 98: 3237-3242.
54. Kucic, N., H. Mahmutefendic, and P. Lucin. 2005. Inhibition of protein kinases C prevents murine cytomegalovirus replication. J. Gen. Virol. 86: 2153-2161.
55. Morello, C. S., L. D. Cranmer, and D. H. Spector. 2000. Suppression of murine cytomegalovirus (MCMV) replication with a DNA vaccine encoding MCMV M84 (a homolog of human cytomegalovirus pp65). J. Virol. 74: 3696-3708.
56. Michel, D., and T. Mertens. 2004. The UL97 protein kinase of human cytomegalovirus and homologues in other herpesviruses: impact on virus and host. Biochim. Biophys. Acta 1697: 169-180.
57. pk) gene. Virology 233: 358-363.
58. Scott, G. M., H. L. Ng, C. J. Morton, M. W. Parker, and W. D. Rawlinson. 2005. Murine cytomegalovirus resistant to antivirals has genetic correlates with human cytomegalovirus. J. Gen. Virol. 86: 2141-2151.
59. Wagner, M., D. Michel, P. Schaarschmidt, B. Vaida, S. Jonjic, M. Messerle, T. Mertens, and U. Koszinowski. 2000. Comparison between human cytomegalovirus pUL97 and murine cytomegalovirus (MCMV) pM97 expressed by MCMV and vaccinia virus: pM97 does not confer ganciclovir sensitivity. J. Virol. 74: 10729-10736.
60. Scalzo, A. A., C. A. Forbes, N. J. Davis-Poynter, H. E. Farrell, and P. A. Lyons. 1995. DNA sequence and transcriptional analysis of the glycoprotein M gene of murine cytomegalovirus. J. Gen. Virol. 76: 2895-2901 (Pt 11).
61. Angulo, A., P. Ghazal, and M. Messerle. 2000. The major immediate-early gene ie3 of mouse cytomegalovirus is essential for viral growth. J. Virol. 74: 11129-11136.
62. Keil, G. M., A. Ebeling-Keil, and U. H. Koszinowski. 1987. Immediate-early genes of murine cytomegalovirus: location, transcripts, and translation products. J. Virol. 61: 526-533.
63. Koszinowski, U. H., M. J. Reddehase, G. M. Keil, and J. Schickedanz. 1987. Host immune response to cytomegalovirus: products of transfected viral immediate-early genes are recognized by cloned cytolytic T lymphocytes. J. Virol. 61: 2054-2058.
64. Manning, W. C., and E. S. Mocarski. 1988. Insertional mutagenesis of the murine cytomegalovirus genome: one prominent α gene (ie2) is dispensable for growth. Virology 167: 477-484.
65. Martinotti, M. G., G. Gribaudo, M. Gariglio, A. Caliendo, D. Lembo, A. Angeretti, R. Cavallo, and S. Landolfo. 1993. Effect of interferon-α on immediate early gene expression of murine cytomegalovirus. J. Interferon Res. 13: 105-109.
66. Messerle, M., B. Buhler, G. M. Keil, and U. H. Koszinowski. 1992. Structural organization, expression, and functional characterization of the murine cytomegalovirus immediate-early gene 3. J. Virol. 66: 27-36.
67. Sandford, G. R., K. Ho, and W. H. Burns. 1993. Characterization of the major locus of immediate-early genes of rat cytomegalovirus. J. Virol. 67: 4093-4103.
68. Hanson, L. K., B. L. Dalton, Z. Karabekian, H. E. Farrell, W. D. Rawlinson, R. M. Stenberg, and A. E. Campbell. 1999. Transcriptional analysis of the murine cytomegalovirus HindIII-I region: identification of a novel immediate-early gene region. Virology 260: 156-164.
69. Hanson, L. K., J. S. Slater, Z. Karabekian, G. Ciocco-Schmitt, and A. E. Campbell. 2001. Products of US22 genes M140 and M141 confer efficient replication of murine cytomegalovirus in macrophages and spleen. J. Virol. 75: 6292-6302.
70. Hanson, L. K., J. S. Slater, Z. Karabekian, H. W. Virgin 4th, C. A. Biron, M. C. Ruzek, N. van Rooijen, R. P. Ciavarra, R. M. Stenberg, and A. E. Campbell. 1999. Replication of murine cytomegalovirus in differentiated macrophages as a determinant of viral pathogenesis. J. Virol. 73: 5970-5980.
71. Karabekian, Z., L. K. Hanson, J. S. Slater, N. K. Krishna, L. L. Bolin, J. A. Kerry, and A. E. Campbell. 2005. Complex formation among murine cytomegalovirus US22 proteins encoded by genes M139, M140, and M141. J. Virol. 79: 3525-3535.
72. d haplotype. J. Virol. 76: 151-164.
73. Pahl-Seibert, M. F., M. Juelch, J. Podlech, D. Thomas, P. Deegen, M. J. Reddehase, and R. Holtappels. 2005. Highly protective in vivo function of cytomegalovirus IE1 epitope-specific memory CD8 T cells purified by T-cell receptor-based cell sorting. J. Virol. 79: 5400-5413.