Importance of antibody in virus infection and vaccine-mediated protection by a latency-deficient recombinant murine γ-herpesvirus-68

Journal of Immunology

Volumn 188, Issue 3, 2012, Pages 1049-1056

  Freeman, Michael L ^a   Burkum, Claire E ^a   Woodland, David L ^a   Sun, Ren ^b   Wu, Ting Ting ^b   Blackman, Marcia A ^a  

^a TRUDEAU INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AC REPLICATION AND TRANSCRIPTION ACTIVATOR; UNCLASSIFIED DRUG; VIRUS ANTIBODY; VIRUS VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GAMMA HERPESVIRUS 68; GAMMA HERPESVIRUS 68 INFECTION; GAMMAHERPESVIRINAE; HUMORAL IMMUNITY; IMMUNITY; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE DEPLETION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTECTION; REAL TIME POLYMERASE CHAIN REACTION; T LYMPHOCYTE; VACCINATION; VIRUS INFECTION; VIRUS REACTIVATION; WILD TYPE;

ANIMALS; ANTIBODIES, VIRAL; IMMUNITY; MICE; MICE, INBRED C57BL; RHADINOVIRUS; T-LYMPHOCYTES; VACCINATION; VACCINES; VACCINES, ATTENUATED; VIRUS ACTIVATION; VIRUS DISEASES; VIRUS LATENCY;

EID: 84856587352     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102621     Document Type: Article

References (48)

1. Barton, E. S., D. W. White, J. S. Cathelyn, K. A. Brett-McClellan, M. Engle, M. S. Diamond, V. L. Miller, and H. W. Virgin, IV. 2007. Herpesvirus latency confers symbiotic protection from bacterial infection. Nature 447: 326-329. (Pubitemid 46788830)
2. Wu, T. T., M. A. Blackman, and R. Sun. 2010. Prospects of a novel vaccination strategy for human gamma-herpesviruses. Immunol. Res. 48: 122-146.
3. Rickinson, A. B., and E. Kieff. 2001. Epstein-Barr Virus. In Fields Virology. P. M. Howley, and D. M. Knipe, eds. Lippincott Williams and Wilkins, Philadelphia, p. 2575-2627.
4. Virgin, H.W., IV, 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 gammaherpesvirus 68. J. Virol. 71: 5894-5904. (Pubitemid 27304926)
5. Nash, A. A., B. M. Dutia, J. P. Stewart, and A. J. Davison. 2001. Natural history of murine gamma-herpesvirus infection. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356: 569-579. (Pubitemid 32442753)
6. Doherty, P. C., J. P. Christensen, G. T. Belz, P. G. Stevenson, and M. Y. Sangster. 2001. Dissecting the host response to a gamma-herpesvirus. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356: 581-593.
7. Sokal, E. M., K. Hoppenbrouwers, C. Vandermeulen, M. Moutschen, P. Léonard, A. Moreels, M. Haumont, A. Bollen, F. Smets, and M. Denis. 2007. Recombinant gp350 vaccine for infectious mononucleosis: a phase 2, randomized, double-blind, placebo-controlled trial to evaluate the safety, immunogenicity, and efficacy of an Epstein-Barr virus vaccine in healthy young adults. J. Infect. Dis. 196: 1749-1753. (Pubitemid 351411934)
8. Stewart, J. P., N. Micali, E. J. Usherwood, L. Bonina, and A. A. Nash. 1999. Murine gamma-herpesvirus 68 glycoprotein 150 protects against virus-induced mononucleosis: a model system for gamma-herpesvirus vaccination. Vaccine 17: 152-157. (Pubitemid 28494114)
9. Liu, L., E. Flaño, 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. (Pubitemid 29328096)
10. Stevenson, P. G., G. T. Belz, M. R. Castrucci, J. D. Altman, and P. C. Doherty. 1999. A gamma-herpesvirus sneaks through a CD8(+) T cell response primed to a lytic-phase epitope. Proc. Natl. Acad. Sci. USA 96: 9281-9286. (Pubitemid 29374746)
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, IV. 2003. Establishment and maintenance of gammaherpesvirus latency are independent of infective dose and route of infection. J. Virol. 77: 7696-7701. (Pubitemid 36734542)
12. Coleman, H. M., B. de Lima, V. Morton, and P. G. Stevenson. 2003. Murine gammaherpesvirus 68 lacking thymidine kinase shows severe attenuation of lytic cycle replication in vivo but still establishes latency. J. Virol. 77: 2410-2417. (Pubitemid 36222764)
13. Flaño, E., Q. Jia, J. Moore, D. L. Woodland, R. Sun, and M. A. Blackman. 2005. Early establishment of gamma-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 gammaherpesvirus 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. (Pubitemid 43134115)
15. Usherwood, E. J., D. J. Roy, K. Ward, S. L. Surman, B. M. Dutia, M. A. Blackman, J. P. Stewart, and D. L. Woodland. 2000. Control of gammaherpesvirus latency by latent antigen-specific CD8(+) T cells. J. Exp. Med. 192: 943-952.
16. Usherwood, E. J., K. A. Ward, M. A. Blackman, J. P. Stewart, and D. L. Woodland. 2001. Latent antigen vaccination in a model gammaherpesvirus infection. J. Virol. 75: 8283-8288. (Pubitemid 32743700)
17. Tibbetts, S. A., J. S. McClellan, S. Gangappa, S. H. Speck, and H. W. Virgin, IV. 2003. Effective vaccination against long-term gammaherpesvirus latency. J. Virol. 77: 2522-2529. (Pubitemid 36222776)
18. Kayhan, B., E. J. Yager, K. Lanzer, T. Cookenham, Q. Jia, T.-T. Wu, D. L. Woodland, R. Sun, and M. A. Blackman. 2007. A replication-deficient murine gamma-herpesvirus blocked in late viral gene expression can establish latency and elicit protective cellular immunity. J. Immunol. 179: 8392-8402.
19. Tibbetts, S. A., F. Suarez, A. L. Steed, J. A. Simmons, and H.W. Virgin, IV. 2006. A gamma-herpesvirus deficient in replication establishes chronic infection in vivo and is impervious to restriction by adaptive immune cells. Virology 353: 210-219. (Pubitemid 44308490)
20. Boname, J. M., H. M. Coleman, J. S. May, and P. G. Stevenson. 2004. Protection against wild-type murine gammaherpesvirus-68 latency by a latency-deficient mutant. J. Gen. Virol. 85: 131-135. (Pubitemid 38128877)
21. Fowler, P., and S. Efstathiou. 2004. Vaccine potential of a murine gammaherpesvirus-68 mutant deficient for ORF73. J. Gen. Virol. 85: 609-613. (Pubitemid 38379862)
22. 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 gammaherpesvirus that is protective against secondary infection. J. Virol. 78: 9215-9223. (Pubitemid 39096531)
23. Jia, Q., M. L. Freeman, E. J. Yager, I. McHardy, L. Tong, D. Martinez-Guzman, T. Rickabaugh, S. Hwang, M. A. Blackman, R. Sun, and T. T. Wu. 2010. Induction of protective immunity against murine gammaherpesvirus 68 infection in the absence of viral latency. J. Virol. 84: 2453-2465.
24. Freeman, M. L., K. G. Lanzer, T. Cookenham, B. Peters, J. Sidney, T. T. Wu, R. Sun, D. L. Woodland, A. Sette, and M. A. Blackman. 2010. Two kinetic patterns of epitope-specific CD8 T-cell responses following murine gammaherpesvirus 68 infection. J. Virol. 84: 2881-2892.
25. Cardin, R. D., J. W. Brooks, S. R. Sarawar, and P. C. Doherty. 1996. Progressive loss of CD8+ T cell-mediated control of a gamma-herpesvirus in the absence of CD4+ T cells. J. Exp. Med. 184: 863-871.
26. Kim, I. J., E. Flaño, D. L. Woodland, and M. A. Blackman. 2002. Antibody-mediated control of persistent gamma-herpesvirus infection. J. Immunol. 168: 3958-3964. (Pubitemid 34298400)
27. Stevenson, P. G., and P. C. Doherty. 1998. Kinetic analysis of the specific host response to a murine gammaherpesvirus. J. Virol. 72: 943-949. (Pubitemid 28116871)
28. Obar, J. J., S. Fuse, E. K. Leung, S. C. Bellfy, and E. J. Usherwood. 2006. Gammaherpesvirus persistence alters key CD8 T-cell memory characteristics and enhances antiviral protection. J. Virol. 80: 8303-8315. (Pubitemid 44384844)
29. Yager, E. J., I. J. Kim, M. L. Freeman, K. G. Lanzer, C. E. Burkum, T. Cookenham, D. L. Woodland, and M. A. Blackman. 2010. Differential impact of ageing on cellular and humoral immunity to a persistent murine gammaherpesvirus. Immun. Ageing 7: 3.
30. -/- mice are agammaglobulinemic and fail to maintain B220-CD138+ plasma cells. J. Immunol. 178: 2192-2203.
31. Carragher, D. M., D. A. Kaminski, A. Moquin, L. Hartson, and T. D. Randall. 2008. A novel role for non-neutralizing antibodies against nucleoprotein in facilitating resistance to influenza virus. J. Immunol. 181: 4168-4176.
32. Flaño, E., S. M. Husain, J. T. Sample, D. L. Woodland, and M. A. Blackman. 2000. Latent murine gamma-herpesvirus infection is established in activated B cells, dendritic cells, and macrophages. J. Immunol. 165: 1074-1081. (Pubitemid 30484779)
33. Flaño, E., I. J. Kim, D. L. Woodland, and M. A. Blackman. 2002. Gammaherpesvirus latency is preferentially maintained in splenic germinal center and memory B cells. J. Exp. Med. 196: 1363-1372. (Pubitemid 35375555)
34. Muramatsu, M., K. Kinoshita, S. Fagarasan, S. Yamada, Y. Shinkai, and T. Honjo. 2000. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102: 553-563.
35. Boes, M., C. Esau, M. B. Fischer, T. Schmidt, M. Carroll, and J. Chen. 1998. Enhanced B-1 cell development, but impaired IgG antibody responses in mice deficient in secreted IgM. J. Immunol. 160: 4776-4787. (Pubitemid 28215311)
36. Terry, L. A., J. P. Stewart, A. A. Nash, and J. K. Fazakerley. 2000. Murine gammaherpesvirus-68 infection of and persistence in the central nervous system. J. Gen. Virol. 81: 2635-2643.
37. Cho, H. J., S. Kim, S. E. Kwak, T. C. Kang, H. S. Kim, H. J. Kwon, Y. W. Kim, Y. S. Kim, E. K. Choi, and M. J. Song. 2009. Age-dependent pathogenesis of murine gammaherpesvirus 68 infection of the central nervous system. Mol. Cells 27: 105-111.
38. Häusler, M., B. Sellhaus, S. Scheithauer, M. Engler, E. Alberg, A. Teubner, K. Ritter, and M. Kleines. 2005. Murine gammaherpesvirus-68 infection of mice: A new model for human cerebral Epstein-Barr virus infection. Ann. Neurol. 57: 600-603. (Pubitemid 40471178)
39. Morrison, L. A., and D. M. Knipe. 1997. Contributions of antibody and T cell subsets to protection elicited by immunization with a replication-defective mutant of herpes simplex virus type 1. Virology 239: 315-326. (Pubitemid 28105638)
40. Stevenson, P. G., R. D. Cardin, J. P. Christensen, and P. C. Doherty. 1999. Immunological control of a murine gammaherpesvirus independent of CD8+ T cells. J. Gen. Virol. 80: 477-483. (Pubitemid 29095210)
41. Gulley, M. L., and W. Tang. 2008. Laboratory assays for Epstein-Barr virus-related disease. J. Mol. Diagn. 10: 279-292. (Pubitemid 352022708)
42. Di Carlo, P., M. Trizzino, L. Titone, G. Capra, P. Colletti, G. Mazzola, D. Pistoia, and C. Sarno. 2011. Unusual MRI findings in an immunocompetent patient with EBV encephalitis: a case report. BMC Med. Imaging 11: 6.
43. Volpi, A. 2004. Epstein-Barr virus and human herpesvirus type 8 infections of the central nervous system. Herpes 11(Suppl 2): 120A-127A.
44. Chan, P. K., H. K. Ng, J. L. Cheung, and A. F. Cheng. 2000. Survey for the presence and distribution of human herpesvirus 8 in healthy brain. J. Clin. Microbiol. 38: 2772-2773. (Pubitemid 30485171)
45. Kapadia, S. B., B. Levine, S. H. Speck, and H. W. Virgin, IV. 2002. Critical role of complement and viral evasion of complement in acute persistent, and latent gamma-herpesvirus infection. Immunity 17: 143-155. (Pubitemid 35245957)
46. Kapadia, S. B., H. Molina, V. van Berkel, S. H. Speck, and H. W. Virgin, IV. 1999. Murine gammaherpesvirus 68 encodes a functional regulator of complement activation. J. Virol. 73: 7658-7670. (Pubitemid 29383250)
47. Tarakanova, V. L., J. M. Molleston, M. Goodwin, and H. W. Virgin, IV. 2010. MHV68 complement regulatory protein facilitates MHV68 replication in primary macrophages in a complement independent manner. Virology 396: 323-328.
48. Weck, K. E., S. S. Kim, H.W. Virgin, IV, and S. H. Speck. 1999. Macrophages are the major reservoir of latent murine gammaherpesvirus 68 in peritoneal cells. J. Virol. 73: 3273-3283. (Pubitemid 29135720)