In vivo replication, latency, and immunogenicity of murine cytomegalovirus mutants with deletions in the M83 and M84 genes, the putative homologs of human cytomegalovirus pp65 (UL83)

Journal of Virology

Volumn 73, Issue 9, 1999, Pages 7678-7693

  Morello, Christopher S ^a   Cranmer, Lee D ^b,c   Spector, Deborah H ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOMEGALOVIRUS VACCINE; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CYTOMEGALOVIRUS; GENE DELETION; HUMAN CYTOMEGALOVIRUS; IMMUNIZATION; IMMUNOGENICITY; INTRAPERITONEAL DRUG ADMINISTRATION; MOUSE; MURINE CYTOMEGALOVIRUS; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS INFECTION; VIRUS LATENCY; VIRUS MUTANT; VIRUS REPLICATION;

EID: 0032816326     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.9.7678-7693.1999     Document Type: Article

References (64)

1. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1993. Current protocols in molecular biology. Greene Publishing Associates and Wiley-Interscience, New York, N.Y.
2. Baldick, C. J., Jr., and T. Shenk. 1996. Proteins associated with purified human cytomegalovirus particles. J. Virol. 70:6097-6105.
3. Balthesen, M., L. Dreher, P. Lucin, and M. J. Reddehase. 1994. The establishment of cytomegalovirus latency in organs is not linked to local virus production during primary infection. J. Gen. Virol. 75:2329-2336.
4. Balthesen, M., M. Messerle, and M. J. Reddehase. 1993. Lungs are a major organ site of cytomegalovirus latency and recurrence. J. Virol. 67:5360-5366.
5. Beninga, J., B. Kropff, and M. Mach. 1995. Comparative analysis of fourteen individual human cytomegalovirus proteins for helper T cell response. J. Gen. Virol. 76:153-160.
6. Bevan, I. S., C. C. Sammons, and C. Sweet. 1996. Investigation of murine cytomegalovirus latency and reactivation in mice using viral mutants and the polymerase chain reaction. J. Med. Virol. 48:308-320.
7. Boname, J. M., and J. K. Chantler. 1992. Characterization of a strain of murine cytomegalovirus which fails to grow in the salivary glands of mice. J. Gen. Virol. 73:2021-2029.
8. Booss, J., and E. F. Wheelock. 1975. Correlation of survival from murine cytomegalovirus infection with spleen cell responsiveness to concanavalin A. Proc. Soc. Exp. Biol. Med. 149:443-445.
9. Boppana, S. B., and W. J. Britt. 1996. Recognition of human cytomegalovirus (HCMV) gene products by HCMV-specific cytotoxic T cells. Virology 222:293-296.
10. Britt, W. J., and D. Auger. 1986. Human cytomegalovirus virion-associated protein with kinase activity. J. Virol. 59:185-188.
11. Collins, T., C. Pomeroy, and M. C. Jordan. 1993. Detection of latent cytomegalovirus DNA in diverse organs of mice. J. Infect. Dis. 168:725-729.
12. Cranmer, L. D., C. Clark, and D. H. Spector. 1994. Cloning, characterization, and expression of the murine cytomegalovirus homologue of the human cytomegalovirus 28-kDa matrix phosphoprotein (UL99). Virology 205:417-429.
13. Cranmer, L. D., C. L. Clark, C. S. Morello, H. E. Farrell, W. D. Rawlinson, and D. H. Spector. 1996. Identification, analysis, and evolutionary relationships of the putative murine cytomegalovirus homologs of the human cytomegalovirus UL82 (pp71) and UL83 (pp65) matrix phosphoproteins. J. Virol. 70:7929-7939.
14. Crnković-Mertens, I., M. Messerle, I. Milotić, U. Szepan, N. Kučić, A. Krmpotić, S. Jonjić, and U. H. Koszinowski. 1998. Virus attenuation after deletion of the cytomegalovirus Fc receptor gene is not due to antibody control. J. Virol. 72:1377-1382.
15. Elliott, R., C. Clark, D. Jaquish, and D. H. Spector. 1991. Transcription analysis and sequence of the putative murine cytomegalovirus DNA polymerase gene. Virology 185:169-186.
16. Farrell, H. E., H. Vally, D. M. Lynch, P. Fleming, G. R. Shellam, A. A. Scalzo, and N. J. Davis-Poynter. 1997. Inhibition of natural killer cells by a cytomegalovirus MHC class I homologue in vivo. Nature 386:510-514.
17. Gallina, A., E. Percivalle, L. Simoncini, M. G. Revello, G. Gerna, and G. Milanesi. 1996. Human cytomegalovirus pp65 lower matrix phosphoprotein harbours two transplantable nuclear localization signals. J. Gen. Virol. 77: 1151-1157.
18. Gallina, A., L. Simoncini, S. Garbelli, E. Percivalle, G. Pedrali-Noy, K. S. Lee, R. L. Erikson, B. Plachter, G. Gerna, and G. Milanesi. 1999. Polo-like kinase 1 as a target for human cytomegalovirus pp65 lower matrix protein. J. Virol. 73:1468-1478.
19. Gebert, S., S. Schmolke, G. Sorg, S. Flöss, B. Plachter, and T. Stamminger. 1997. The UL84 protein of human cytomegalovirus acts as a transdominant inhibitor of immediate-early-mediated transactivation that is able to prevent viral replication. J. Virol. 71:7048-7060.
20. Gilbert, M. J., S. R. Riddell, B. Plachter, and P. D. Greenberg. 1996. Cytomegalovirus selectively blocks antigen processing and presentation of its immediate-early gene product. Nature 383:720-722.
21. González Armas, J. C., C. S. Morello, L. D. Cranmer, and D. H. Spector. 1996. DNA immunization confers protection against murine cytomegalovirus infection. J. Virol. 70:7921-7928.
22. Grundy, J. E., J. S. Mackenzie, and N. F. Stanley. 1981. Influence of H-2 and non-H-2 genes on resistance to murine cytomegalovirus infection. Infect. Immun. 32:277-286.
23. Harlow, E., and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
24. Hayashi, K., Y. Eizuru, S. Sato, and Y. Minamishima. 1985. The role of NK cell activity in age-dependent resistance of mice to murine cytomegalovirus infection. Microbiol. Immunol. 29:939-950.
25. He, Y. S., L. Xu, and E.-S. Huang. 1992. Characterization of human cytomegalovirus UL84 early gene and identification of its putative protein product. J. Virol. 66:1098-1108.
26. Hengel, H., and U. H. Koszinowski. 1997. Interference with antigen processing by viruses. Curr. Opin. Immunol. 9:470-476.
27. Henry, S. C., and J. D. Hamilton. 1993. Detection of murine cytomegalovirus immediate early 1 transcripts in the spleens of latently infected mice. J. Infect. Dis. 167:950-954.
28. Ho, M. 1992. Cytomegalovirus biology and infection, 2nd ed. Plenum Medical Book Co., New York, N.Y.
29. Holtappels, R., J. Podlech, G. Geginat, H.-P. Steffens, D. Thomas, and M. J. Reddehase. 1998. Control of murine cytomegalovirus in the lungs: relative but not absolute immunodominance of the immediate-early 1 nonapeptide during the antiviral cytolytic T-lymphocyte response in pulmonary infiltrates. J. Virol. 72:7201-7212.
30. Jahn, G., B. C. Scholl, B. Traupe, and B. Fleckenstein. 1987. The two major structural phosphoproteins (pp65 and pp150) of human cytomegalovirus and their antigenic properties. J. Gen. Virol. 68:1327-1337.
31. Jordan, M. C., and J. L. Takagi. 1983. Virulence characteristics of murine cytomegalovirus in cell and organ cultures. Infect. Immun. 41:841-843.
32. Koffron, A. J., M. Hummel, B. K. Patterson, S. Yan, D. B. Kaufman, J. P. Fryer, F. P. Stuart, and M. I. Abecassis. 1998. Cellular localization of latent murine cytomegalovirus. J. Virol. 72:95-103.
33. Koszinowski, U. H., M. J. Reddehase, and M. Del Val. 1992. Principles of cytomegalovirus antigen presentation in vitro and in vivo. Semin. Immunol. 4:71-79.
34. Kurz, S., H.-P. Steffens, A. Mayer, J. R. Harris, and M. J. Reddehase. 1997. Latency versus persistence or intermittent recurrences: evidence for a latent state of murine cytomegalovirus in the lungs. J. Virol. 71:2980-2987.
35. Lagenaur, L. A., W. C. Manning, J. Vieira, C. L. Martens, and E. S. Mocarski. 1994. Structure and function of the murine cytomegalovirus sggl gene: a determinant of viral growth in salivary gland acinar cells. J. Virol. 68:7717-7727.
36. Lathbury, L. J., J. E. Allan, G. R. Shellam, and A. A. Scalzo. 1996. Effect of host genotype in determining the relative roles of natural killer cells and T cells in mediating protection against murine cytomegalovirus infection. J. Gen. Virol. 77:2605-2613.
37. MacDonald, M. R., X.-Y. Li, R. M. Stenberg, A. E. Campbell, and H. W. Virgin IV. 1998. Mucosal and parenteral vaccination against acute and latent murine cytomegalovirus (MCMV) infection by using an attenuated MCMV mutant. J. Virol. 72:442-451.
38. Manning, W. C., C. A. Stoddart, L. A. Lagenaur, G. B. Abenes, and E. S. Mocarski. 1992. Cytomegalovirus determinant of replication in salivary glands. J. Virol. 66:3794-3802.
39. + virus-specific cytotoxic T lymphocytes. J. Med. Virol. 43:103-110.
40. Mercer, J. A., J. R. Marks, and D. H. Spector. 1983. Molecular cloning and restriction endonuclease mapping of the murine cytomegalovirus genome (Smith strain). Virology 129:94-106.
41. Mercer, J. A., C. A. Wiley, and D. H. Spector. 1988. Pathogenesis of murine cytomegalovirus infection: identification of infected cells in the spleen during acute and latent infections. J. Virol. 62:987-997.
42. Mims, C. A., and J. Gould. 1978. Splenic necrosis in mice infected with cytomegalovirus. J. Infect. Dis. 137:587-591.
43. Morello, C. S., L. D. Cranmer, and D. H. Spector. Unpublished data.
44. Pollock, J. L., and H. W. Virgin IV. 1995. Latency, without persistence, of murine cytomegalovirus in the spleen and kidney. J. Virol. 69:1762-1768.
45. Pomeroy, C., P. J. Hilleren, and M. C. Jordan. 1991. Latent murine cytomegalovirus DNA in splenic stromal cells of mice. J. Virol. 65:3330-3334.
46. Prichard, M., and G. Pari. Personal communication.
47. Quinnan, G. V., Jr., N. Kirmani, E. Esber, R. Saral, J. F. Manischewitz, J. L. Rogers, A. H. Rook, G. W. Santos, and W. H. Burns. 1981. HLA-restricted cytotoxic T lymphocyte and nonthymic cytotoxic lymphocyte responses to cytomegalovirus infection of bone marrow transplant recipients. J. Immunol. 126:2036-2041.
48. Quinnan, G. V., Jr., N. Kirmani, A. H. Rook, J. F. Manischewitz, L. Jackson, G. Moreschi, G. W. Santos, R. Saral, and W. H. Burns. 1982. Cytotoxic T cells in cytomegalovirus infection: HLA-restricted T-lymphocyte and non-T-lymphocyte cytotoxic responses correlate with recovery from cytomegalovirus infection in bone-marrow-transplant recipients. N. Engl. J. Med. 307:7-13.
49. 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.
50. Reddehase, M. J., M. Balthesen, M. Rapp, S. Jonjic, I. Pavic, and U. H. Koszinowski. 1994. The conditions of primary infection define the load of latent viral genome in organs and the risk of recurrent cytomegalovirus disease. J. Exp. Med. 179:185-193.
51. Reddehase, M. J., H.-J. Bühring, and U. H. Koszinowski. 1986. Cloned long-term cytolytic T-lymphocyte line with specificity for an immediate-early membrane antigen of murine cytomegalovirus. J. Virol. 57:408-412.
52. Reddehase, M. J., G. M. Keil, and U. H. Koszinowski. 1984. The cytolytic T lymphocyte response to the murine cytomegalovirus. II. Detection of virus replication stage-specific antigens by separate populations of in vivo active cytolytic T lymphocyte precursors. Eur. J. Immunol. 14:56-61.
53. Reusser, P., S. R. Riddell, J. D. Meyers, and P. D. Greenberg. 1991. Cytotoxic T-lymphocyte response to cytomegalovirus after human allogeneic bone marrow transplantation: pattern of recovery and correlation with cytomegalovirus infection and disease. Blood 78:1373-1380.
54. Sambrook, J., E. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
55. Sarisky, R. T., and G. S. Hayward. 1996. Evidence that the UL84 gene product of human cytomegalovirus is essential for promoting oriLyt-dependent DNA replication and formation of replication compartments in cotransfection assays. J. Virol. 70:7398-7413.
56. Schmolke, S., P. Drescher, G. Jahn, and B. Plachter. 1995. Nuclear targeting of the tegument protein pp65 (UL83) of human cytomegalovirus: an unusual bipartite nuclear localization signal functions with other portions of the protein to mediate its efficient nuclear transport. J. Virol. 69:1071-1078.
57. Schmolke, S., H. F. Kern, P. Drescher, G. Jahn, and B. Plachter. 1995. The dominant phosphoprotein pp65 (UL83) of human cytomegalovirus is dispensable for growth in cell culture. J. Virol. 69:5959-5968.
58. Spaete, R. R., and E. S. Mocarski. 1987. Insertion and deletion mutagenesis of the human cytomegalovirus genome. Proc. Natl. Acad. Sci. USA 84:7213-7217.
59. Spector, D. J., and M. J. Tevethia. 1994. Protein-protein interactions between human cytomegalovirus IE2-580aa and pUL84 in lytically infected cells. J. Virol. 68:7549-7553.
60. Steffens, H.-P., S. Kurz, R. Holtappels, and M. J. Reddehase. 1998. Preemptive CD8 T-cell immunotherapy of acute cytomegalovirus infection prevents lethal disease, limits the burden of latent viral genomes, and reduces the risk of virus recurrence. J. Virol. 72:1797-1804.
61. Stoddart, C. A., R. D. Cardin, J. M. Boname, W. C. Manning, G. B. Abenes, and E. S. Mocarski. 1994. Peripheral blood mononuclear phagocytes mediate dissemination of murine cytomegalovirus. J. Virol. 68:6243-6253.
62. van Zanten, J., M. C. Harmsen, P. van der Meer, W. van der Bij, W. J. van Son, M. van der Giessen, J. Prop, L. de Leij, and T. H. The. 1995. Proliferative T cell responses to four human cytomegalovirus-specific proteins in healthy subjects and solid organ transplant recipients. J. Infect. Dis. 172: 879-882.
63. Vieira, J., H. E. Farrell, W. D. Rawlinson, and E. S. Mocarski. 1994. Genes in the HindIII J fragment of the murine cytomegalovirus genome are dispensable for growth in cultured cells: insertion mutagenesis with a lacZ/gpt cassette. J. Virol. 68:4837-4846.
64. Wills, M. R., A. J. Carmichael, K. Mynard, X. Jin, M. P. Weekes, B. Plachter, and J. G. P. Sissons. 1996. The human cytotoxic T-lymphocyte (CTL) response to cytomegalovirus is dominated by structural protein pp65: frequency, specificity, and T-cell receptor usage of pp65-specific CTL. J. Virol. 70:7569-7579.