Circulating specific antibodies enhance systemic cross-priming by delivery of complexed antigen to dendritic cells in vivo

European Journal of Immunology

Volumn 42, Issue 3, 2012, Pages 598-606

  van Montfoort, Nadine ^a,d   Mangsbo, Sara M ^a   Camps, Marcel G M ^a   van Maren, Wendy W C ^a   Verhaart, Ingrid E C ^a   Waisman, Ari ^b   Drijfhout, Jan Wouter ^a   Melief, Cornelis J M ^a,c   Verbeek, J Sjef ^a   Ossendorp, Ferry ^a,d  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c ISA Pharmaceuticals   (Netherlands)

^d ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Antibodies; B cells; Cross presentation; Dendritic cells; Tcells

Indexed keywords

ANTIBODY; ANTIGEN; GLYCOPROTEIN P 15095; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; T LYMPHOCYTE ANTIGEN;

ANIMAL EXPERIMENT; ANTIBODY SPECIFICITY; ANTIGEN ANTIBODY COMPLEX; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS PRESENTATION; DENDRITIC CELL; HUMORAL IMMUNITY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGEN-ANTIBODY COMPLEX; ANTIGENS, CD11C; ANTIGENS, NEOPLASM; CD8-POSITIVE T-LYMPHOCYTES; CROSS-PRIMING; DENDRITIC CELLS; FLOW CYTOMETRY; HAPTENS; HISTOCOMPATIBILITY ANTIGENS CLASS I; IMMUNITY, CELLULAR; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; OVALBUMIN; SERUM ALBUMIN, BOVINE;

EID: 84859486381     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201141613     Document Type: Article

References (34)

1. Qin, Z., Richter, G., Schuler, T., Ibe, S., Cao, X. and Blankenstein, T., B cells inhibit induction of T-cell dependent tumor immunity. Nat. Med. 1998. 4: 627-630.
2. Shah, S., Divekar, A. A., Hilchey, S. P., Cho, H. M., Newman, C. L., Shin, S. U., Nechustan, H. et al., Increased rejection of primary tumors in mice lacking B cells: inhibition of anti-tumor CTL and TH1 cytokine responses by B cells. Int. J. Cancer 2005. 117: 574-586.
3. DiLillo, D. J., Yanaba, K. and Tedder, T. F., 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. 2010. 184: 4006-4016.
4. Weiner, L. M., Dhodapkar, M. V. and Ferrone, S., Monoclonal antibodies for cancer immunotherapy. Lancet 2009. 373: 1033-1040.
5. de Bono, J. S., Rha, S. Y., Stephenson, J., Schultes, B. C., Monroe, P., Eckhardt, G. S., Hammond, L. A. et al., Phase I trial of a murine antibody to MUC1 in patients with metastatic cancer: evidence for the activation of humoral and cellular antitumor immunity. Ann. Oncol. 2004. 15: 1825-1833.
6. Taylor, C., Hershman, D., Shah, N., Suciu-Foca, N., Petrylak, D. P., Taub, R., Vahdat, L. et al., Augmented HER-2 specific immunity during treatment with trastuzumab and chemotherapy. Clin. Cancer Res. 2007. 13: 5133-5143.
7. Kim, P. S., Armstrong, T. D., Song, H., Wolpoe, M. E., Weiss, V., Manning, E. A., Huang, L. Q. et al., Antibody association with HER-2/neu-targeted vaccine enhances CD8 T cell responses in mice through Fc-mediated activation of DCs. J. Clin. Invest 2008. 118: 1700-1711.
8. Hjelm, F., Carlsson, F., Getahun, A. and Heyman, B., Antibody-mediated regulation of the immune response. Scand. J. Immunol. 2006. 64: 177-184.
9. Getahun, A., Dahlstrom, J., Wernersson, S. and Heyman, B., IgG2a-mediated enhancement of antibody and T cell responses and its relation to inhibitory and activating Fc gamma receptors. J. Immunol. 2004. 172: 5269-5276.
10. Michaud, H. A., Gomard, T., Gros, L., Thiolon, K., Nasser, R., Jacquet, C., Hernandez, J. et al., A crucial role for infected-cell/antibody immune complexes in the enhancement of endogenous antiviral immunity by short passive immunotherapy. PLoS Pathog. 2010. 6: e1000948.
11. Regnault, A., Lankar, D., Lacabanne, V., Rodriguez, A., Thery, C., Rescigno, M., Saito, T. et al., Fcgamma receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization. J. Exp. Med. 1999. 189: 371-380.
12. Schuurhuis, D.H., Ioan-Facsinay, A., Nagelkerken, B., van Schip, J. J., Sedlik, C., Melief, C. J., Verbeek, J. S. et al., Antigen-antibody immune complexes empower dendritic cells to efficiently prime specific CD8+ CTL responses in vivo. J. Immunol. 2002. 168: 2240-2246.
13. van Montfoort, N., de Jong, J. M., Schuurhuis, D. H., van der Voort, E. I., Camps, M. G., Huizinga, T. W., van Kooten, C. et al., A novel role of complement factor C1q in augmenting the presentation of antigen captured in immune complexes to CD8+ Tlymphocytes. J. Immunol. 2007. 178: 7581-7586.
14. de Jong, J. M., Schuurhuis, D. H., Ioan-Facsinay, A., Welling, M. M., Camps, M. G., van der Voort, E. I., Huizinga, T. W. et al., Dendritic cells, but not macrophages or B cells, activate major histocompatibility complex class II-restricted CD4+ T cells upon immune-complex uptake in vivo. Immunology 2006. 119: 499-506.
15. Schuurhuis, D. H., van Montfoort, N., Ioan-Facsinay, A., Jiawan, R., Camps, M., Nouta, J., Melief, C. J. et al., Immune complex-loaded dendritic cells are superior to soluble immune complexes as antitumor vaccine. J. Immunol. 2006. 176: 4573-4580.
16. van Montfoort, N., Camps, M. G., Khan, S., Filippov, D. V., Weterings, J. J., Griffith, J. M., Geuze, H. J. et al., Antigen storage compartments in mature dendritic cells facilitate prolonged cytotoxic T lymphocyte cross-priming capacity. Proc. Natl. Acad. Sci. USA 2009. 106: 6730-6735.
17. Baudino, L., Nimmerjahn, F., Azeredo da Silveira, S., Martinez-Soria, E., Saito, T., Carroll, M., Ravetch, J. V. et al., Differential contribution of three activating IgG Fc receptors (FcgammaRI, FcgammaRIII, and FcgammaRIV) to IgG2a- and IgG2b-induced autoimmune hemolytic anemia in mice. J. Immunol. 2008. 180: 1948-1953.
18. Nimmerjahn, F. and Ravetch, J. V., Fcgamma receptors as regulators of immune responses. Nat. Rev. Immunol. 2008. 8: 34-47.
19. Caton, M. L., Smith-Raska, M .R. and Reizis, B., Notch-RBP-Jsignaling controls the homeostasis of CD8- dendritic cells in the spleen. J. Exp. Med. 2007. 204: 1653-1664.
20. Buch, T., Heppner, F. L., Tertilt, C., Heinen, T. J., Kremer, M., Wunderlich, F. T., Jung, S. et al., A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat. Methods 2005. 2: 419-426.
21. Hjelm, F., Karlsson, M. C. and Heyman, B., A novel B cell-mediated transport of IgE-immune complexes to the follicle of the spleen. J. Immunol. 2008. 180: 6604-6610.
22. Pulendran, B., Tang, H., and Denning, T. L., Division of labor, plasticity, and crosstalk between dendritic cell subsets. Curr. Opin. Immunol. 2008. 20: 61-67.
23. Villadangos, J. A. and Schnorrer, P., Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat. Rev. Immunol. 2007. 7: 543-555.
24. den Haan, J. M. and Bevan, M. J., Constitutive versus activation-dependent cross-presentation of immune complexes by CD8(+) and CD8(-) dendritic cells in vivo. J. Exp. Med. 2002. 196: 817-827.
25. Flores, M., Desai, D. D., Downie, M., Liang, B., Reilly, M. P., McKenzie, S. E. and Clynes, R., Dominant expression of the inhibitory FcgammaRIIB prevents antigen presentation by murine plasmacytoid dendritic cells. J. Immunol. 2009. 183: 7129-7139.
26. den Haan, J. M., Lehar, S. M. and Bevan, M. J., CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J. Exp. Med. 2000. 192: 1685-1696.
27. Germain, R. N., Bajenoff, M., Castellino, F., Chieppa, M., Egen, J. G., Huang, A. Y., Ishii, M. et al., Making friends in out-of-the-way places: how cells of the immune system get together and how they conduct their business as revealed by intravital imaging. Immunol. Rev. 2008. 221: 163-181.
28. Roozendaal, R., Mempel, T. R., Pitcher, L. A., Gonzalez, S. F., Verschoor, A., Mebius, R. E., von Andrian, U. H. et al., Conduits mediate transport of low-molecular-weight antigen to lymph node follicles. Immunity 2009. 30: 264-276.
29. Sixt, M., Kanazawa, N., Selg, M., Samson, T., Roos, G., Reinhardt, D. P., Pabst, R. et al., The conduit system transports soluble antigens from the afferent lymph to resident dendritic cells in the T cell area of the lymph node. Immunity 2005. 22: 19-29.
30. Jung, S., Unutmaz, D., Wong, P., Sano, G., De los, S. K., Sparwasser, T., Wu, S. et al., In vivo depletion of CD11c(+) dendritic cells abrogates priming of CD8(+) T cells by exogenous cell-associated antigens. Immunity. 2002. 17: 211-220.
31. Delamarre, L., Pack, M., Chang, H., Mellman, I. and Trombetta, E.S., Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 2005. 307: 1630-1634.
32. Perreau, M., Pantaleo, G. and Kremer, E. J., Activation of a dendritic cell-Tcell axis by Ad5 immune complexes creates an improved environment for replication of HIV in T cells. J. Exp. Med. 2008. 205: 2717-2725.
33. Saenger, Y. M., Li, Y., Chiou, K. C., Chan, B., Rizzuto, G., Terzulli, S. L., Merghoub, T. et al., Improved tumor immunity using anti-tyrosinase related protein-1 monoclonal antibody combined with DNA vaccines in murine melanoma. Cancer Res. 2008. 68: 9884-9891.
34. Park, S., Jiang, Z., Mortenson, E. D., Deng, L., Radkevich-Brown, O., Yang, X., Sattar, H. et al., The therapeutic effect of anti-HER/neu antibody depends on both innate and adaptive immunity. Cancer Cell 2010. 18: 160-170.