Optimal long-term humoral responses to replication-defective herpes simplex virus require CD21/CD35 complement receptor expression on stromal cells

Journal of Virology

Volumn 80, Issue 14, 2006, Pages 7111-7117

  Brockman, Mark A ^a,c   Verschoor, Admar ^a,b,d   Zhu, Jia ^a,e   Carroll, Michael C ^a,b   Knipe, David M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b CENTER FOR BLOOD RESEARCH   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d INSTITUTE OF EXPERIMENTAL IMMUNOLOGY   (Switzerland)

^e Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; COMPLEMENT COMPONENT C3B RECEPTOR; COMPLEMENT COMPONENT C3D RECEPTOR; IMMUNOGLOBULIN G; VIRUS ANTIGEN; VIRUS DNA; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; HERPES SIMPLEX VIRUS; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; STROMA CELL; VERO CELL; VIRUS REPLICATION; WESTERN BLOTTING;

ANIMALS; ANTIBODIES, VIRAL; ANTIBODY FORMATION; ANTIGENS, VIRAL; B-LYMPHOCYTES; BONE MARROW TRANSPLANTATION; CERCOPITHECUS AETHIOPS; COMPLEMENT SYSTEM PROTEINS; DENDRITIC CELLS; HERPES SIMPLEX VIRUS VACCINES; HERPESVIRUS 2, HUMAN; HUMANS; IMMUNOGLOBULIN G; IMMUNOLOGIC MEMORY; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; NEURONS; RECEPTORS, COMPLEMENT 3B; RECEPTORS, COMPLEMENT 3D; STROMAL CELLS; TIME FACTORS; TRANSPLANTATION CHIMERA; VERO CELLS; VIRUS LATENCY; VIRUS REPLICATION;

ANIMALIA; SIMPLEXVIRUS;

EID: 33745770407     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01421-05     Document Type: Article

References (39)

1. Ahearn, J. M., M. B. Fischer, D. Croix, S. Goerg, M. Ma, J. Xia, X. Zhou, R. G. Howard, T. L. Rothstein, and M. C. Carroll. 1996. Disruption of the Cr2 locus results in a reduction in B-1a cells and in an impaired B cell response to T-dependent antigen. Immunity 4:251-262.
2. Bachmann, M. F., T. M. Kundig, H. Hengartner, and R. M. Zinkernagel. 1994. Regulation of IgG antibody titers by the amount persisting of immune-complexed antigen. Eur. J. Immunol. 24:2567-2570.
3. Bachmann, M. F., B. Odermatt, H. Hengartner, and R. M. Zinkernagel. 1996. Induction of long-lived germinal centers associated with persisting antigen after viral infection. J. Exp. Med. 183:2259-2269.
4. Barrington, R. A., O. Pozdnyakova, M. R. Zafari, C. D. Benjamin, and M. C. Carroll. 2002. B lymphocyte memory: role of stromal cell complement and FcgRIIB receptors. J. Exp. Med. 196:1189-1199.
5. Boursnell, M. E., C. Entwisle, D. Blakeley, C. Roberts, I. A. Duncan, S. E. Chisholm, G. M. Martin, R. Jennings, D. Ni Challanain, I. Sobek, S. C. Inglis, and C. S. McLean. 1997. A genetically inactivated herpes simplex virus type 2 (HSV-2) vaccine provides effective protection against primary and recurrent disease. J. Infect. Dis. 175:16-25.
6. + cytotoxic T-lymphocyte response and confers a level of protection comparable to that of wild-type HSV-1. J. Virol. 71:3534-3544.
7. Brockman, M. A., and D. M. Knipe. 2002. Herpes simplex virus vectors elicit durable immune responses in the presence of preexisting host immunity. J. Virol. 76:3678-3687.
8. -/- mice: enhanced affinity maturation but impaired antibody persistence. J. Immunol. 164:4522-4532.
9. DaCosta, X., M. F. Kramer, J. Zhu, M. A. Brockman, and D. M. Knipe. 2000. Construction, phenotypic analysis, and immunogenicity of a UL5/UL29 double deletion mutant of herpes simplex virus 2. J. Virol. 74:7963-7971.
10. DaCosta, X. J., N. Bourne, L. R. Stanberry, and D. M. Knipe. 1997. Construction and characterization of a replication-defective herpes simplex virus 2 ICP8 mutant strain and its use in immunization studies in a guinea pig model of genital disease. Virology 232:1-12.
11. DaCosta, X. J., M. A. Brockman, E. Alicot, M. Ma, M. B. Fischer, X. Zhou, D. M. Knipe, and M. C. Carroll. 1999. Humoral response to herpes simplex virus is complement dependent. Proc. Natl. Acad. Sci. USA 96:12708-12712.
12. DaCosta, X. J., C. A. Jones, and D. M. Knipe. 1999. Immunization against genital herpes with a vaccine virus that has defects in productive and latent infection. Proc. Natl. Acad. Sci. USA 96:6994-6998.
13. Fang, Y., C. Xu, Y. X. Fu, V. M. Holers, and H. Molina. 1998. Expression of complement receptors 1 and 2 on follicular dendritic cells is necessary for the generation of a strong antigen-specific IgG response. J. Immunol. 160:5273-5279.
14. Fayette, J., I. Durand, J. M. Bridon, C. Arpin, B. Dubois, C. Caux, Y. J. Liu, J. Banchereau, and F. Briere. 1998. Dendritic cells enhance the differentiation of naive B cells into plasma cells in vitro. Scand. J. Immunol. 48:563-570.
15. Fischer, M. B., M. Ma, N. C. Hsu, and M. C. Carroll. 1998. Local synthesis of C3 within the splenic lymphoid compartment can reconstitute the impaired immune response in C3-deficient mice. J. Immunol. 160:2619-2625.
16. Hoshino, Y., S. K. Dalai, K. Wang, L. Pesniak, T. Y. Lau, D. M. Knipe, J. I. Cohen, and S. E. Straus. 2005. Comparative efficacy and immunogenicity of replication-defective, recombinant glycoprotein and DNA vaccines for herpes simplex virus 2 infections in mice and guinea pigs. J. Virol. 79:410-418.
17. Jones, C. A., T. J. Taylor, and D. M. Knipe. 2000. Biological properties of herpes simplex virus 2 replication-defective mutant strains in a murine nasal infection model. Virology 278:137-150.
18. Klaus, G. G. B., J. H. Humphrey, A. Kunkl, and D. W. Dongworth. 1980. The follicular dendritic cell: its role in antigen presentation in the generation of immunological memory. Immunol. Rev. 53:3-59.
19. Knipe, D. M., and A. E. Spang. 1982. Definition of a series of stages in the association of two herpesviral proteins with the cell nucleus. J. Virol. 43:314-324.
20. Kramer, M. F., and D. M. Coen. 1995. Quantification of transcripts from the ICP4 and thymidine kinase genes in mouse ganglia latently infected with herpes simplex virus. J. Virol. 69:1389-1399.
21. Leib, D. A., D. M. Coen, C. L. Bogard, K. A. Hicks, D. R. Yager, D. M. Knipe, K. L. Tyler, and P. A. Schaffer. 1989. Immediate-early regulatory gene mutants define different stages in the establishment and reactivation of herpes simplex virus latency. J. Virol. 63:759-768.
22. Ludewig, B., K. J. Maloy, C. Lopez-Macias, B. Odermatt, H. Hengartner, and R. M. Zinkernagel. 2000. Induction of optimal anti-viral neutralizing B cell responses by dendritic cells requires transport and release of virus particles in secondary lypmphoid organs. Eur. J. Immunol. 30:185-196.
23. Manz, R. A., M. Lohning, G. Cassese, A. Theil, and A. Radbruch. 1998. Survival of long-lived plasma cells is independent of antigen. Int. Immunol. 10:1703-1711.
24. Maruyama, M., K. P. Lam, and K. Rajewsky. 2000. Memory B-cell persistence is independent of persisting immunizing antigen. Nature 407:636-642.
25. McLean, C. S., M. Erturk, R. Jennings, D. N. Challanain, A. C. Minson, M. E. Boursnell, and S. C. Inglis. 1994. Protective vaccination against primary and recurrent disease caused by herpes simplex virus (HSV) type 2 using a genetically disabled HSV-1. J. Infect. Dis. 170:1100-1109.
26. McLean, C. S., D. Ni Challanain, I. A. Duncan, M. E. Boursnell, R. Jennings, and S. C. Inglis. 1996. Induction of a protective immune response by mucosal vaccination with a DISC HSV-1 vaccine. Vaccine 14:987-992.
27. Molina, H., V. M. Holers, B. Li, Y. Fung, S. Mariathasan, J. Goellner, J. Strauss-Schoenberger, R. W. Karr, and D. D. Chaplin. 1996. Markedly impaired humoral immune response in mice deficient in complement receptors 1 and 2. Proc. Natl. Acad. Sci. USA 93:3357-3361.
28. Morrison, L. A., X. J. DaCosta, and D. M. Knipe. 1998. Influence of mucosal and parenteral immunization with a replication-defective mutant of HSV-2 on immune responses and protection from genital challenge. Virology 243:178-187.
29. Morrison, L. A., and D. M. Knipe. 1994. Immunization with replication-defective mutants of herpes simplex virus type 1: sites of immune intervention in pathogenesis of challenge virus infection. J. Virol. 68:689-696.
30. Morrison, L. A., and D. M. Knipe. 1996. Mechanisms of immunization with a replication-defective mutant of herpes simplex virus 1. Virology 220:402-413.
31. 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.
32. Murphy, C. G., W. T. Lucas, R. E. Means, S. Czajak, C. L. Hale, J. D. Lifson, A. Kaur, R. P. Johnson, D. M. Knipe, and R. C. Desrosiers. 2000. Vaccine protection against simian immunodeficiency virus by recombinant strains of herpes simplex virus. J. Virol. 74:7745-7754.
33. Qin, D., J. Wu, K. A. Vora, J. V. Ravetch, A. K. Szakal, T. Manser, and J. G. Tew. 2000. Fc gamma receptor IIB on follicular dendritic cells regulates the B cell recall response. J. Immunol. 164:6268-6275.
34. Slifka, M. K., and R. Ahmed. 1998. Long-lived plasma cells: a mechanism for maintaining persistent antibody production. Curr. Opin. Immunol. 10:252-258.
35. Slifka, M. K., R. Anitia, J. K. Whitmire, and R. Ahmed. 1998. Humoral immunity due to long-lived plasma cells. Immunity 8:363-372.
36. van den Berg, T. K., E. A. Dopp, M. R. Daha, G. Kraal, and C. D. Dijkstra. 1992. Selective inhibition of immune complex trapping by follicular dendritic cells with monoclonal antibodies against rat C3. Eur. J. Immunol. 22:957-962.
37. Verschoor, A., M. A. Brockman, M. Gadjeva, D. M. Knipe, and M. C. Carroll. 2003. Myeloid C3 determines induction of humoral responses to peripheral herpes simplex virus infection. J. Immunol. 171:5363-5371.
38. Verschoor, A., M. A. Brockman, D. M. Knipe, and M. C. Carroll. 2001. Cutting edge: myeloid complement C3 enhances the humoral response to peripheral viral infection. J. Immunol. 167:2446-2451.
39. Yoshida, K., T. K. van den Berg, and C. D. Dijkstra. 1993. Two functionally different follicular dendritic cells in secondary lymphoid follicles of mouse spleen, as revealed by CR1/2 and FcR gamma II-mediated immune-complex trapping. Immunology 80:34-39.