A replication-deficient murine γ-herpesvirus blocked in late viral gene expression can establish latency and elicit protective cellular immunity

Journal of Immunology

Volumn 179, Issue 12, 2007, Pages 8392-8402

  Kayhan, Basak ^a   Yager, Eric J ^a   Lanzer, Kathleen ^a   Cookenham, Tres ^a   Jia, Qingmei ^b   Wu, Ting Ting ^b   Woodland, David L ^a   Sun, Ren ^b   Blackman, Marcia A ^a  

^a TRUDEAU INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BAGG ALBINO MOUSE; C57BL 6 MOUSE; CELLULAR IMMUNITY; DENDRITIC CELL; FLOW CYTOMETRY; HERPES VIRUS; HISTOPATHOLOGY; IMMUNOGENICITY; IMMUNOREGULATION; INOCULATION; LATENT PERIOD; MACROPHAGE; MOUSE; NONHUMAN; PERSISTENT INFECTION; PRIORITY JOURNAL; VACCINATION; VIRUS EXPRESSION; VIRUS GENE; VIRUS LOAD; VIRUS REPLICATION; ANIMAL; BLOOD; C57BL MOUSE; GENE EXPRESSION REGULATION; GENETICS; HERPES VIRUS INFECTION; IMMUNOLOGY; LUNG; PERITONEUM; PHYSIOLOGY; SPLEEN; VIROLOGY; VIRUS LATENCY;

HERPES VACCINE; VIRUS ANTIBODY;

ANIMALS; ANTIBODIES, VIRAL; B-LYMPHOCYTES; GAMMAHERPESVIRINAE; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRIDAE INFECTIONS; HERPESVIRUS VACCINES; IMMUNITY, CELLULAR; LUNG; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PERITONEUM; SPLEEN; VIRAL LOAD; VIRUS LATENCY; VIRUS REPLICATION;

EID: 40049111562     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.12.8392     Document Type: Article

References (59)

1. Stevenson, P. G. 2004. Immune evasion by γ-herpesviruses. Curr. Opin. Immunol. 16: 456-462.
2. Nash, A. A., B. M. Dutia, J. P. Stewart, and A. J. Davison. 2001. Natural history of murine γherpesvirus infection. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356: 569-579.
3. Doherty, P. C., J. P. Christensen, G. T. Belz, P. G. Stevenson, and M. Y. Sangster. 2001. Dissecting the host response to a γ-herpesvirus. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356: 581-593.
4. Virgin, H. W. 2005. Immune regulation of viral infection and vice versa. Immunol. Res. 32: 293-315.
5. Stevenson, P. G., and S. Efstathiou. 2005. Immune mechanisms in murine γherpesvirus-68 infection. Viral Immunol. 18: 445-456.
6. Blackman, M. A., and E. Flano. 2002. Persistent γ-herpesvirus infections: what can we learn from an experimental mouse model? J. Exp. Med. 195: F29-32.
7. Liu, L., E. J. Usherwood, M. A. Blackman, and D. L. Woodland. 1999. T-cell vaccination alters the course of murine herpesvirus 68 infection and the establishment of viral latency in mice. J. Virol. 73: 9849-9857.
8. + T cell response primed to a lytic-phase epitope. Proc. Natl. Acad. Sci. USA 96: 9281-9286.
9. Usherwood, E. J., K. A. Ward, M. A. Blackman, J. P. Stewart, and D. L. Woodland. 2001. Latent antigen vaccination in a model γherpesvirus infection. J. Virol. 75: 8283-8288.
10. Stewart, J. P., N. J. Janjua, S. D. Pepper, G. Bennion, M. Mackett, T. Allen, A. A. Nash, and J. R. Arrand. 1996. Identification and characterization of murine γherpesvirus 68 gp150: a virion membrane glycoprotein. J. Virol. 70: 3528-3535.
11. Tibbetts, S. A., J. Loh, V. Van Berkel, J. S. McClellan, M. A. Jacoby, S. B. Kapadia, S. H. Speck, and H. W. Virgin. 2003. Establishment and maintenance of γherpesvirus latency are independent of infective dose and route of infection. J. Virol. 77: 7696-7701.
12. Coleman, H. M., B. de Lima, V. Morton, and P. G. Stevenson. 2003. Murine γherpesvirus 68 lacking thymidine kinase shows severe attenuation of lytic cycle replication in vivo but still establishes latency. J. Virol. 77: 2410-2417.
13. Flano, E., Q. Jia, J. Moore, D. L. Woodland, R. Sun, and M. A. Blackman. 2005. Early establishment of γ-herpesvirus latency: implications for immune control. J. Immunol. 174: 4972-4978.
14. Moser, J. M., M. L. Farrell, L. T. Krug, J. W. Upton, and S. H. Speck. 2006. A γherpesvirus 68 gene 50 null mutant establishes long-term latency in the lung but fails to vaccinate against a wild-type virus challenge. J. Virol. 80: 1592-1598.
15. Tibbetts, S. A., J. S. McClellan, S. Gangappa, S. H. Speck, and H. W. Virgin. 2003. Effective vaccination against long-Term γherpesvirus latency. J. Virol. 77: 2522-2529.
16. Rickabaugh, T. M., H. J. Brown, D. Martinez-Guzman, T. T. Wu, L. Tong, F. Yu, S. Cole, and R. Sun. 2004. Generation of a latency-deficient γherpesvirus that is protective against secondary infection. J. Virol. 78: 9215-9223.
17. Boname, J. M., H. M. Coleman, J. S. May, and P. G. Stevenson. 2004. Protection against wild-type murine γherpesvirus-68 latency by a latency-deficient mutant. J. Gen. Virol. 85: 131-135.
18. Fowler, P., and S. Efstathiou. 2004. Vaccine potential of a murine γherpesvirus-68 mutant deficient for ORF73. J. Gen. Virol. 85: 609-613.
19. Tibbetts, S. A., F. Suarez, A. L. Steed, J. A. Simmons, and H. W. Virgin. 2006. A γ-herpesvirus deficient in replication establishes chronic infection in vivo and is impervious to restriction by adaptive immune cells. Virology 353: 210-219.
20. Liu, S., I. V. Pavlova, H. W. Virgin, and S. H. Speck. 2000. Characterization of γherpesvirus 68 gene 50 transcription. J. Virol. 74: 2029-2037.
21. Pavlova, I. V., H. W. Virgin, and S. H. Speck. 2003. Disruption of γherpesvirus 68 gene 50 demonstrates that Rta is essential for virus replication. J. Virol. 77: 5731-5739.
22. Jia, Q., T. T. Wu, H. I. Liao, V. Chernishof, and R. Sun. 2004. Murine γherpesvirus 68 open reading frame 31 is required for viral replication. J. Virol. 78: 6610-6620.
23. Virgin, H. W., P. Latreille, P. Wamsley, K. Hallsworth, K. E. Weck, A. J. Dal Canto, and S. H. Speck. 1997. Complete sequence and genomic analysis of murine γherpesvirus 68. J. Virol. 71: 5894-5904.
24. + T cells. J. Exp. Med. 184: 863-871.
25. Flano, E., B. Kayhan, D. L. Woodland, and M. A. Blackman. 2005. Infection of dendritic cells by a γ 2-herpesvirus induces functional modulation. J. Immunol. 175: 3225-3234.
26. Weck, K. E., M. L. Barkon, L. I. Yoo, S. H. Speck, and H. W. Virgin. 1996. Mature B cells are required for acute splenic infection, but not for establishment of latency, by murine γherpesvirus 68. J. Virol. 70: 6775-6780.
27. Kim, I. J., E. Flano, D. L. Woodland, and M. A. Blackman. 2002. Antibody-mediated control of persistent γ-herpesvirus infection. J. Immunol. 168: 3958-3964.
28. + T-cell response to a persistent γherpesvirus. J. Virol. 73: 4279-4283.
29. Adler, H., M. Messerle, and U. H. Koszinowski. 2001. Virus reconstituted from infectious bacterial artificial chromosome (BAC)-cloned murine γherpesvirus 68 acquires wild-type properties in vivo only after excision of BAC vector sequences. J. Virol. 75: 5692-5696.
30. Flano, E., S. M. Husain, J. T. Sample, D. L. Woodland, and M. A. Blackman. 2000. Latent murine γ-herpesvirus infection is established in activated B cells, dendritic cells, and macrophages. J. Immunol. 165: 1074-1081.
31. Sunil-Chandra, N. P., S. Efstathiou, and A. A. Nash. 1992. Murine γherpesvirus 68 establishes a latent infection in mouse B lymphocytes in vivo. J. Gen. Virol. 73: 3275-3279.
32. Flano, E., I. J. Kim, D. L. Woodland, and M. A. Blackman. 2002. γ-Herpesvirus latency is preferentially maintained in splenic germinal center and memory B cells. J. Exp. Med. 196: 1363-1372.
33. Willer, D. O., and S. H. Speck. 2003. Long-term latent murine γherpesvirus 68 infection is preferentially found within the surface immunoglobulin D-negative subset of splenic B cells in vivo. J. Virol. 77: 8310-8321.
34. Marques, S., S. Efstathiou, K. G. Smith, M. Haury, and J. P. Simas. 2003. Selective gene expression of latent murine γherpesvirus 68 in B lymphocytes. J. Virol. 77: 7308-7318.
35. Gangappa, S., S. B. Kapadia, S. H. Speck, and H. W. Virgin. 2002. Antibody to a lytic cycle viral protein decreases γherpesvirus latency in B-cell-deficient mice. J. Virol. 76: 11460-11468.
36. + T lymphocytes. Proc. Natl. Acad. Sci. USA 96: 7508-7513.
37. Sparks-Thissen, R. L., D. C. Braaten, S. Kreher, S. H. Speck, and H. W. Virgin. 2004. An optimized CD4 T-cell response can control productive and latent γherpesvirus infection. J. Virol. 78: 6827-6835.
38. McClellan, J. S., S. A. Tibbetts, S. Gangappa, K. A. Brett, and H. W. Virgin. 2004. Critical role of CD4 T cells in an antibody-independent mechanism of vaccination against γherpesvirus latency. J. Virol. 78: 6836-6845.
39. + T cell-mediated control of a γ-herpesvirus in B cell- deficient mice is mediated by IFN-γ. Proc. Natl. Acad. Sci. USA 96: 5135-5140.
40. + T cell response during acute and persistent murine γ-herpesvirus infection. Eur. J. Immunol. 29: 1059-1067.
41. Usherwood, E. J., J. P. Stewart, K. Robertson, D. J. Allen, and A. A. Nash. 1996. Absence of splenic latency in murine γherpesvirus 68-infected B cell-deficient mice. J. Gen. Virol. 77: 2819-2825.
42. Stewart, J. P., E. J. Usherwood, A. Ross, H. Dyson, and T. Nash. 1998. Lung epithelial cells are a major site of murine γherpesvirus persistence. J. Exp. Med. 187: 1941-1951.
43. Liu, L., E. Flano, E. J. Usherwood, S. Surman, M. A. Blackman, and D. L. Woodland. 1999. Lytic cycle T cell epitopes are expressed in two distinct phases during MHV-68 infection. J. Immunol. 163: 868-874.
44. Ehtisham, S., N. P. Sunil-Chandra, and A. A. Nash. 1993. Pathogenesis of murine γherpesvirus infection in mice deficient in CD4 and CD8 T cells. J. Virol. 67: 5247-5252.
45. Rooney, C. M., C. A. Smith, C. Y. Ng, S. Loftin, C. Li, R. A. Krance, M. K. Brenner, and H. E. Heslop. 1995. Use of gene-modified virus-specific T lymphocytes to control Epstein-Barr-virus-related lymphoproliferation. Lancet 345: 9-13.
46. + T cells. J. Exp. Med. 192: 943-952.
47. Stevenson, P. G., S. Efstathiou, P. C. Doherty, and P. J. Lehner. 2000. Inhibition of MHC class I-restricted antigen presentation by γ 2- herpesviruses. Proc. Natl. Acad. Sci. USA 97: 8455-8460.
48. Van Berkel, V., J. Barrett, H. L. Tiffany, D. H. Fremont, P. M. Murphy, G. McFadden, S. H. Speck, and H. W. Virgin. 2000. Identification of a γherpesvirus selective chemokine binding protein that inhibits chemokine action. J. Virol. 74: 6741-6747.
49. Parry, C. M., J. P. Simas, V. P. Smith, C. A. Stewart, A. C. Minson, S. Efstathiou, and A. Alcami. 2000. A broad spectrum secreted chemokine binding protein encoded by a herpesvirus. J. Exp. Med. 191: 573-578.
50. Bridgeman, A., P. G. Stevenson, J. P. Simas, and S. Efstathiou. 2001. A secreted chemokine binding protein encoded by murine γherpesvirus- 68 is necessary for the establishment of a normal latent load. J. Exp. Med. 194: 301-312.
51. Epstein, M. A., A. J. Morgan, S. Finerty, B. J. Randle, and J. K. Kirkwood. 1985. Protection of cottontop tamarins against Epstein-Barr virus-induced malignant lymphoma by a prototype subunit vaccine. Nature 318: 287-289.
52. Stewart, J. P., N. Micali, E. J. Usherwood, L. Bonina, and A. A. Nash. 1999. Murine γ-herpesvirus 68 glycoprotein 150 protects against virus- induced mononucleosis: a model system for γ-herpesvirus vaccination. Vaccine 17: 152-157.
53. Gillet, L., M. B. Gill, S. Colaco, C. M. Smith, and P. G. Stevenson. 2006. Murine γherpesvirus-68 glycoprotein B presents a difficult neutralization target to monoclonal antibodies derived from infected mice. J. Gen. Virol. 87: 3515-3527.
54. Gill, M. B., L. Gillet, S. Colaco, J. S. May, B. de Lima, and P. G. Stevenson. 2006. Murine γherpesvirus-68 glycoprotein H-glycoprotein L complex is a major target for neutralizing monoclonal antibodies. J. Gen. Virol. 87: 1465-1475.
55. Parren, P. W., and D. R. Burton. 2001. The antiviral activity of antibodies in vitro and in vivo. Adv. Immunol. 77: 195-262.
56. Roth, M. G., and R. W. Compans. 1980. Antibody-resistant spread of vesicular stomatitis virus infection in cell lines of epithelial origin. J. Virol. 35: 547-550.
57. De Lima, B., J. S. May, and P. G. Stevenson. 2004. Murine γherpesvirus 68 lacking gp150 shows defective virion release but establishes normal latency in vivo. J. Virol. 78: 5103-5112.
58. Stewart, J. P., O. J. Silvia, I. M. Atkin, D. J. Hughes, B. Ebrahimi, and H. Adler. 2004. In vivo function of a γherpesvirus virion glycoprotein: influence on B-cell infection and mononucleosis. J. Virol. 78: 10449-10459.
59. May, J. S., J. Walker, S. Colaco, and P. G. Stevenson. 2005. The murine γherpesvirus 68 ORF27 gene product contributes to intercellular viral spread. J. Virol. 79: 5059-5068.