Immune evasion proteins enhance cytomegalovirus latency in the lungs

Journal of Virology

Volumn 83, Issue 19, 2009, Pages 10293-10298

  Böhm, Verena ^a   Seckert, Christof K ^a   Simon, Christian O ^a   Thomas, Doris ^a   Renzaho, Angélique ^a   Gendig, Dorothea ^a   Holtappels, Rafaela ^a   Reddehase, Matthias J ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GLYCOPROTEIN; IMMUNE EVASION PROTEIN; UNCLASSIFIED DRUG; VIRUS DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; BONE MARROW TRANSPLANTATION; CD8+ T LYMPHOCYTE; CELL STIMULATION; CYTOMEGALOVIRUS; GENE DELETION; INTERSTITIAL PNEUMONIA; MEMBRANE RECONSTITUTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS GENE; VIRUS GENOME; VIRUS LATENCY; VIRUS LOAD; VIRUS REACTIVATION; VIRUS TRANSCRIPTION;

ANIMALS; ANTIGEN-PRESENTING CELLS; BONE MARROW CELLS; CD8-POSITIVE T-LYMPHOCYTES; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; FEMALE; GENOME, VIRAL; GLYCOPROTEINS; LUNG; MICE; MICE, INBRED BALB C; RECURRENCE; TRANSCRIPTION, GENETIC; VIRUS LATENCY;

CYTOMEGALOVIRUS; MURINAE;

EID: 70349289131     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01143-09     Document Type: Article

References (47)

1. Arase, H., E. S. Mocarski, A. E. Campbell, A. B. Hill, and L. L. Lanier. 2002. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296:1323-1326. (Pubitemid 34522789)
2. 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. (Pubitemid 23241369)
3. Böhm, V., J. Podlech, D. Thomas, P. Deegen, M.-F. Pahl-Seibert, N. A. W. Lemmermann, N. K. A. Grzimek, S. A. Oehrlein-Karpi, M. J. Reddehase, and R. Holtappels. 2008. Epitope-specific in vivo protection against cytomegalovirus disease by CD8 T cells in the murine model of preemptive immunotherapy. Med. Microbiol. Immunol. 197:135-144.
4. Böhm, V., C. O. Simon, J. Podlech, C. K. Seckert, D. Gendig, P. Deegen, D. Gillert-Marien, N. A. W. Lemmermann, R. Holtappels, and M. J. Reddehase. 2008. The immune evasion paradox: immunoevasins of murine cytomegalovirus enhance priming of CD8 T cells by preventing negative feedback regulation. J. Virol. 82:11637-11650.
5. Busche, A., A. Marquardt, A. Bleich, P. Ghazal, A. Angulo, and M. Messerle. 2009. The mouse cytomegalovirus immediate-early 1 gene is not required for establishment of latency or for reactivation in the lungs. J. Virol. 83:4030-4038.
6. Cobbold, M., N. Khan, B. Pourgheysari, S. Tauro, D. McDonald, H. Osman, M. Assenmacher, I. Billingham, C. Steward, C. Crawley, E. Olavarria, J. Goldman, R. Chakraverty, P. Mahendra, C. Craddock, and P. A. Moss. 2005. Adoptive transfer of cytomegalovirus-specific CTL to stem cell transplant patients after selection by HLA-peptide tetramers. J. Exp. Med. 202:379-386.
7. del Val, M., H. Hengel, H. Häcker, 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.
8. Doom, C. M., and A. B. Hill. 2008. MHC class I immune evasion in MCMV infection. Med. Microbiol. Immunol. 197:191-204.
9. Emery, V. C. 1998. Relative importance of cytomegalovirus load as a risk factor for cytomegalovirus disease in the immunocompromised host, p. 288-301. In M. Scholz, H. F. Rabenau, H. W. Doerr, and J. Cinatl, Jr. (ed.), CMV-related immunopathology. Monographs in Virology, vol.21. Karger, Basel, Switzerland.
10. Ghazal, P., A. E. Visser, M. Gustems, R. Garcia, E. M. Borst, K. Sullivan, M. Messerle, and A. Angulo. 2005. Elimination of ie1 significantly attenuates murine cytomegalovirus virulence but does not alter replicative capacity in cell culture. J. Virol. 79:7182-7194.
11. 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.
12. 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.
13. Grzimek, N. K. A., D. Dreis, S. Schmalz, and M. J. Reddehase. 2001. Random, asynchronous, and asymmetric transcriptional activity of enhancer-flanking major immediate-early genes ie1/3 and ie2 during murine cytomegalovirus latency in the lungs. J. Virol. 75:2692-2705.
14. Holtappels, R., V. Böhm, J. Podlech, and M. J. Reddehase. 2008. CD8 T-cell-based immunotherapy of cytomegalovirus infection: "proof of concept" provided by the murine model. Med. Microbiol. Immunol. 197:125-134.
15. Holtappels, R., D. Gillert-Marien, D. Thomas, J. Podlech, P. Deegen, S. Herter, S. A. Oehrlein-Karpi, D. Strand, M. Wagner, and M. J. Reddehase. 2006. Cytomegalovirus encodes a positive regulator of antigen presentation. J. Virol. 80:7613-7624. (Pubitemid 44092582)
16. Holtappels, R., M. W. Munks, J. Podlech, and M. J. Reddehase. 2006. CD8 T-cell-based immunotherapy of cytomegalovirus disease in the mouse model of the immunocompromised bone marrow transplantation recipient, p. 383-418. In M. J. Reddehase (ed.), Cytomegaloviruses: molecular biology and immunology. Caister Academic Press, Wymondham, Norfolk, United Kingdom.
17. lo memory-effector cell pool during latent murine cytomegalovirus infection of the lungs. J. Virol. 74:11495-11503.
18. 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. (Pubitemid 28377849)
19. Holtappels, R., J. Podlech, M.-F. Pahl-Seibert, M. Juelch, 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.
20. + T lymphocytes. J. Virol. 64:5457-5464.
21. Jordan, M. C., and V. L. Mar. 1982. Spontaneous activation of latent cytomegalovirus from murine spleen explants: role of lymphocytes and macrophages in release and replication of virus. J. Clin. Investig. 70:762-768.
22. Kurz, S. K., M. Rapp, H.-P. Steffens, N. K. A. Grzimek, S. Schmalz, and M. J. Reddehase. 1999. Focal transcriptional activity of murine cytomegalovirus during latency in the lungs. J. Virol. 73:482-494.
23. Kurz, S. K., and M. J. Reddehase. 1999. Patchwork pattern of transcriptional reactivation in the lungs indicates sequential checkpoints in the transition from murine cytomegalovirus latency to recurrence. J. Virol. 73:8612-8622.
24. Lenac, T., J. Arapovic, L. Traven, A. Krmpotic, and S. Jonjic. 2008. Murine cytomegalovirus regulation of NKG2D ligands. Med. Microbiol. Immunol. 197:159-166.
25. 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.
26. Munks, M. W., A. K. Pinto, C. M. Doom, and A. B. Hill. 2007. Viral interference with antigen presentation does not alter acute or chronic CD8 T cell immunodominance in murine cytomegalovirus infection. J. Immunol. 178:7235-7241.
27. Peggs, K. S., S. Verfuerth, A. Pizzey, N. Khan, M. Gulver, P. A. Moss, and S. Mackinnon. 2003. Adoptive cellular therapy for early cytomegalovirus infection after allogeneic stem-cell transplantation with virus-specific T-cell lines. Lancet 362:1375-1377.
28. Pinto, A. K., M. W. Munks, U. H. Koszinowski, and A. B. Hill. 2006. Coordinated function of murine cytomegalovirus genes completely inhibits CTL lysis. J. Immunol. 177:3225-3234.
29. Podlech, J., R. Holtappels, N. K. A. Grzimek, and M. J. Reddehase. 2002. Animal models: murine cytomegalovirus, p. 493-525. In S. H. E. Kaufmann and D. Kabelitz (ed.), Methods in microbiology, vol.32. Immunology of infection, 2nd ed. Academic Press, London, United Kingdom.
30. Podlech, J., R. Holtappels, M.-F. Pahl-Seibert, H.-P. Steffens, and M. J. Reddehase. 2000. Murine model of interstitial cytomegalovirus pneumonia in syngeneic bone marrow transplantation: persistence of protective pulmonary CD8-T-cell infiltrates after clearance of acute infection. J. Virol. 74:7496-7507. (Pubitemid 30613095)
31. Podlech, J., R. Holtappels, N. Wirtz, H.-P. Steffens, and M. J. Reddehase. 1998. Reconstitution of CD8 T cells is essential for the prevention of multiple-organ cytomegalovirus histopathology after bone marrow transplantation. J. Gen. Virol. 79:2099-2104.
32. Quinnan, G. V., Jr., W. H. Burns, N. Kirmani, A. H. Rook, J. Manischewitz, L. Jackson, G. W. Santos, and R. Sarai. 1984. HLA-restricted cytotoxic T lymphocytes are an early immune response and important defense mechanism in cytomegalovirus infections. Rev. Infect. Dis. 6:156-163.
33. Reddehase, M. J. 2002. Antigens and immunoevasins: opponents in cytomegalovirus immune surveillance. Nat. Rev. Immunol. 2:831-844.
34. 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.
35. Reddehase, M. J., S. Jonjic, F. Weiland, W. Mutter, and U. H. Koszinowski. 1988. Adoptive immunotherapy of murine cytomegalovirus adrenalitis in the immunocompromised host: CD4-helper-independent antiviral function of CD8-positive memory T lymphocytes derived from latently infected donors. J. Virol. 62:1061-1065.
36. Reddehase, M. J., F. Weiland, K. Münch, S. Jonjic, A. Lüske, and U. H. Koszinowski. 1985. Interstitial murine cytomegalovirus pneumonia after irradiation: characterization of cells that limit viral replication during established infection of the lungs. J. Virol. 55:264-273.
37. 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. (Pubitemid 29082286)
38. 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.
39. Riddell, S. R. 1995. Pathogenesis of cytomegalovirus pneumonia in immunocompromised hosts. Semin. Respir. Infect. 10:199-208.
40. Riddell, S. R., K. S. Watanabe, J. M. Goodrich, C. R. Li, M. E. Agha, and P. D. Greenberg. 1992. Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones. Science 257:238-241.
41. Roizmann, N., and A. E. Sears. 1987. An inquiry into the mechanisms of herpes simplex virus latency. Annu. Rev. Microbiol. 41:543-571.
42. Seckert, C. K., A. Renzaho, M. J. Reddehase, and N. K. Grzimek. 2008. Hematopoietic stem cell transplantation with latently infected donors does not transmit virus to immunocompromised recipients in the murine model of cytomegalovirus infection. Med. Microbiol. Immunol. 197:251-259.
43. Simon, C. O., R. Holtappels, H.-M. Tervo, V. Böhm, T. Däubner, S. A. Oehrlein-Karpi, B. Kühnapfel, A. Renzaho, D. Strand, J. Podlech, M. J. Reddehase, and N. K. A. Grzimek. 2006. CD8 T cells control cytomegalovirus latency by epitope-specific sensing of transcriptional reactivation. J. Virol. 80:10436-10456.
44. 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 genome, and reduces the risk of virus recurrence. J. Virol. 72:1797-1804.
45. Wagner, M., A. Gutermann, J. Podlech, M. J. Reddehase, and U. H. Koszinowski. 2002. MHC class I allele-specific cooperative and competitive interactions between immune evasion proteins of cytomegalovirus. J. Exp. Med. 196:805-816.
46. 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. (Pubitemid 29327894)
47. Ziegler, H., R. Thäle, 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. (Pubitemid 27130215)