Complement opsonization enhances Friend virus infection of B cells and thereby amplifies the virus-specific CD8+ T cell response

Journal of Virology

Volumn 85, Issue 2, 2011, Pages 1151-1155

  Bila, Custodio ^a   Oberhauser, Verena ^a   Ammann, Christoph G ^a   Ejaz, Asim ^a   Huber, Georg ^a   Schimmer, Simone ^b   Messer, Ron ^c   Pekna, Marcela ^d   Von Laer, Dorothee ^a   Dittmer, Ulf ^b   Hasenkrug, Kim J ^c   Stoiber, Heribert ^a   Bánki, Zoltán ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF DUISBURG ESSEN   (Germany)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; FRIEND LEUKEMIA VIRUS; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE ACTIVATION; MOUSE; NONHUMAN; OPSONIZATION; PRIORITY JOURNAL; VIRUS INFECTION;

ANIMALS; B-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; COMPLEMENT SYSTEM PROTEINS; FRIEND MURINE LEUKEMIA VIRUS; MICE;

FRIEND MURINE LEUKEMIA VIRUS;

EID: 78650659644     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01821-10     Document Type: Article

References (31)

1. Ammann, C. G., R. J. Messer, K. E. Peterson, and K. J. Hasenkrug. 2009. Lactate dehydrogenase-elevating virus induces systemic lymphocyte activation via TLR7-dependent IFNalpha responses by plasmacytoid dendritic cells. PLoS One 4:e6105.
2. Bajtay, Z., C. Speth, A. Erdei, and M. P. Dierich. 2004. Cutting edge: productive HIV-1 infection of dendritic cells via complement receptor type 3 (CR3, CD11b/CD18). J. Immunol. 173:4775-4778.
3. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392:245-252.
4. Bánki, Z., W. Posch, A. Ejaz, V. Oberhauser, S. Willey, C. Gassner, H. Stoiber, U. Dittmer, M. P. Dierich, K. Hasenkrug, and D. Wilflingseder. 2010. Complement as an endogenous adjuvant for dendritic cell-mediated induction of retrovirus-specific CTLs. PLoS Pathog. 6:e1000891.
5. Bouhlal, H., N. Chomont, M. Réquena, N. Nasreddine, H. Saidi, J. Legoff, M. D. Kazatchkine, L.Bélec, and H. Hocini. 2007. Opsonization of HIV with complement enhances infection of dendritic cells and viral transfer to CD4 T cells in a CR3 and DC-SIGN-dependent manner. J. Immunol. 178:1086-1095.
6. Bowen, D. L., D. D. Isaak, and J. Cerny. 1979. Inhibition of in vitro Friend murine leukemia virus infection of lipopolysaccharide-activated B-cells with concanavalin A. J. Natl. Cancer Inst. 62:1497-1502.
7. Browne, E. P., and D. R. Littman. 2009. Myd88 is required for an antibody response to retroviral infection. PLoS Pathog. 5:e1000298.
8. Cerny, J., P. A. Hensgen, S. H. Fistel, and L. M. Demler. 1976. Interactions of murine leukemia virus (MuLV) with isolated lymphocytes. II. Infections of B and T cells with Friend virus complex in diffusion chambers and in vitro: effect of polyclonal mitogens. Int. J. Cancer 18:189-196.
9. Chen, W., H. Qin, B. Chesebro, and M. A. Cheever. 1996. Identification of a gag-encoded cytotoxic T-lymphocyte epitope from FBL-3 leukemia shared by Friend, Moloney, and Rauscher murine leukemia virus-induced tumors. J. Virol. 70:7773-7782.
10. Coughlin, C. M., B. A. Vance, S. A. Grupp, and R. H. Vonderheide. 2004. RNA-transfected CD40-activated B cells induce functional T-cell responses against viral and tumor antigen targets: implications for pediatric immunotherapy. Blood 103:2046-2054.
11. Crawford, A., M. Macleod, T. Schumacher, L. Corlett, and D. Gray. 2006. Primary T cell expansion and differentiation in vivo requires antigen presentation by B cells. J. Immunol. 176:3498-3506.
12. Delibrias, C. C., A. Mouhoub, E. Fischer, and M. D. Kazatchkine. 1994. CR1(CD35) and CR2(CD21) complement C3 receptors are expressed on normal human thymocytes and mediate infection of thymocytes with opsonized human immunodeficiency virus. Eur. J. Immunol. 24:2784-2788.
13. Delibrias, C. C., M. D. Kazatchkine, and E. Fischer. 1993. Evidence for the role of CR1 (CD35), in addition to CR2 (CD21), in facilitating infection of human T cells with opsonized HIV. Scand. J. Immunol. 38:183-189.
14. DiLillo, D. J., K. Yanaba, and T. F. Tedder. 2010. B cells are required for optimal CD4+ and CD8+ T cell tumor immunity: therapeutic B cell depletion enhances B16 melanoma growth in mice. J. Immunol. 184:4006-4016.
15. Dittmer, U., H. He, R. J. Messer, S. Schimmer, A. R. Olbrich, C. Ohlen, P. D. Greenberg, I. M. Stromnes, M. Iwashiro, S. Sakaguchi, L. H. Evans, K. E. Peterson, et al. 2004. Functional impairment of CD8(+) T cells by regulatory T cells during persistent retroviral infection. Immunity 20:293-303.
16. Gras, G., Y. Richard, P. Roques, R. Olivier, and D. Dormont. 1993. Complement and virus-specific antibody-dependent infection of normal B lymphocytes by human immunodeficiency virus type 1. Blood 81:1808-1818.
17. Hasenkrug, K. J., and U. Dittmer. 2007. Immune control and prevention of chronic Friend retrovirus infection. Front. Biosci. 12:1544-1551.
18. Hasenkrug, K. J., D. M. Brooks, and U. Dittmer. 1998. Critical role for CD4(+) T cells in controlling retrovirus replication and spread in persistently infected mice. J. Virol. 72:6559-6564.
19. Jung, S., D. Unutmaz, P. Wong, G. Sano, K. De los Santos, T. Sparwasser, S. Wu, S. Vuthoori, K. Ko, F. Zavala, E. G. Pamer, D. R. Littman, and R. A. Lang. 2002. In vivo depletion of CD11c(+) dendritic cells abrogates priming of CD8(+) T cells by exogenous cell-associated antigens. Immunity 17:211-220.
20. Probst, H. C., and M. van den Broek. 2005. Priming of CTLs by lymphocytic choriomeningitis virus depends on dendritic cells. J. Immunol. 174:3920-3924.
21. Pruenster, M., D. Wilflingseder, Z. Bánki, C. G. Ammann, B. Muellauer, M. Meyer, C. Speth, M. P. Dierich, and H. Stoiber. 2005. C-type lectin-independent interaction of complement opsonized HIV with monocyte-derived dendritic cells. Eur. J. Immunol. 35:2691-2698.
22. Ritchie, D. S., J. Yang, I. F. Hermans, and F. Ronchese. 2004. B-lymphocytes activated by CD40 ligand induce an antigen-specific anti-tumour immune response by direct and indirect activation of CD8(+) T-cells. Scand. J. Immunol. 60:543-551.
23. Rivera, A., C. C. Chen, N. Ron, J. P. Dougherty, and Y. Ron. 2001. Role of B cells as antigen-presenting cells in vivo revisited: antigen-specific B cells are essential for T cell expansion in lymph nodes and for systemic T cell responses to low antigen concentrations. Int. Immunol. 13:1583-1593.
24. Robertson, S. J., C. G. Ammann, R. J. Messer, A. B. Carmody, L. Myers, U. Dittmer, S. Nair, N. Gerlach, L. H. Evans, W. A. Cafruny, and K. J. Hasenkrug. 2008. Suppression of acute anti-Friend virus CD8+ T-cell responses by coinfection with lactate dehydrogenase-elevating virus. J. Virol. 82:408-418.
25. Schultze, J. L., S. Grabbe, and M. S. von Bergwelt-Baildon. 2004. DCs and CD40-activated B cells: current and future avenues to cellular cancer immunotherapy. Trends Immunol. 25:659-664.
26. Spear, G. T., M. Hart, G. G. Olinger, F. B. Hashemi, and M. Saifuddin. 2001. The role of the complement system in virus infections. Curr. Top. Microbiol. Immunol. 260:229-245.
27. Suzuki, T., S. Aizawa, and H. Ikeda. 2001. Expression of receptor for ecotropic murine leukemia virus on hematopoietic cells. Arch. Virol. 146:507-519.
28. Thieblemont, N., N. Haeffner-Cavaillon, A. Ledur, J. L'Age-Stehr, H. W. Ziegler-Heitbrock, and M. D. Kazatchkine. 1993. CR1 (CD35) and CR3 (CD11b/CD18) mediate infection of human monocytes and monocytic cell lines with complement-opsonized HIV independently of CD4. Clin. Exp. Immunol. 92:106-113.
29. Tsuji-Kawahara, S., T. Chikaishi, E. Takeda, M. Kato, S. Kinoshita, E. Kajiwara, S. Takamura, and M. Miyazawa. 2010. Persistence of viremia and production of neutralizing antibodies differentially regulated by polymorphic APOBEC3 and BAFF-R loci in Friend virus-infected mice. J. Virol. 84:6082-6095.
30. Zelinskyy, G., A. R. Kraft, S. Schimmer, T. Arndt, and U. Dittmer. 2006. Kinetics of CD8+ effector T cell responses and induced CD4+ regulatory T cell responses during Friend retrovirus infection. Eur. J. Immunol. 36:2658-2670.
31. Zelinskyy, G., K. K. Dietze, Y. P. Hüsecken, S. Schimmer, S. Nair, T. Werner, K. Gibbert, O. Kershaw, A. D. Gruber, T. Sparwasser, and U. Dittmer. 2009. The regulatory T-cell response during acute retroviral infection is locally defined and controls the magnitude and duration of the virus-specific cytotoxic T-cell response. Blood 114:3199-3207