Controlling immune responses by targeting antigens to dendritic cell subsets and B cells

International Immunology

Volumn 26, Issue 1, 2014, Pages 3-11

  Chappell, Craig P ^a   Giltiay, Natalia V ^a   Dresch, Christiane ^a   Clark, Edward A ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Antigen targeting; B cell; Dendritic cell; Sntibody

Indexed keywords

ALPHA INTERFERON; ANTIGEN; CD180 ANTIGEN; CD209 ANTIGEN; CD8 ANTIGEN; CD8 ANTIGEN ALPHA; CHEMOKINE RECEPTOR; DECTIN 1; HAPTEN; INTERFERON REGULATORY FACTOR 7; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ANTIGEN TARGETING; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURFACE; CELLULAR IMMUNITY; CROSS PRESENTATION; GENE REARRANGEMENT; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOREGULATION; MYELOID DENDRITIC CELL; MYELOID DENDRITIC CELL SUBSETS; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PLASMACYTOID DENDRITIC CELL SUBSETS; PRIORITY JOURNAL; PROTEIN TARGETING; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; UPREGULATION;

ANTIBODY; ANTIGEN TARGETING; B CELL; DENDRITIC CELL;

ANIMALS; ANTIGEN-PRESENTING CELLS; ANTIGENS; B-LYMPHOCYTES; DENDRITIC CELLS; HUMANS; IMMUNE SYSTEM;

EID: 84893401886     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxt059     Document Type: Article

References (77)

1. Tacken, P. J., Torensma, R. and Figdor, C. G. 2006. Targeting antigens to dendritic cells in vivo. Immunobiology 211:599.
2. Kawamura, H. and Berzofsky, J. A. 1986. Enhancement of antigenic potency in vitro and immunogenicity in vivo by coupling the antigen to anti-immunoglobulin. J. Immunol. 136:58.
3. Bergtold, A., Desai, D. D., Gavhane, A. and Clynes, R. 2005. Cell surface recycling of internalized antigen permits dendritic cell priming of B cells. Immunity 23:503.
4. Chappell, C. P., Draves, K. E., Giltiay, N. V. and Clark, E. A. 2012. Extrafollicular B cell activation by marginal zone dendritic cells drives T cell-dependent antibody responses. J. Exp. Med. 209:1825.
5. Dubois, B. and Caux, C. 2005. Critical role of ITIM-bearing FcgammaR on DCs in the capture and presentation of native antigen to B cells. Immunity 23:463.
6. Wykes, M. and MacPherson, G. 2000. Dendritic cell-B-cell interaction: dendritic cells provide B cells with CD40-independent proliferation signals and CD40-dependent survival signals. Immunology 100:1.
7. Wykes, M., Pombo, A., Jenkins, C. and MacPherson, G. G. 1998. Dendritic cells interact directly with naive B lymphocytes to transfer antigen and initiate class switching in a primary T-dependent response. J. Immunol. 161:1313.
8. Barber, B. H. 1997. The immunotargeting approach to adjuvantindependent subunit vaccine design. Semin. Immunol. 9:293.
9. Lees, A., Morris, S. C., Thyphronitis, G., Holmes, J. M., Inman, J. K. and Finkelman, F. D. 1990. Rapid stimulation of large specific antibody responses with conjugates of antigen and anti-IgD antibody. J. Immunol. 145:3594.
10. Carayanniotis, G. and Barber, B. H. 1987. Adjuvant-free IgG responses induced with antigen coupled to antibodies against class II MHC. Nature 327:59.
11. Casten, L. A., Kaumaya, P. and Pierce, S. K. 1988. Enhanced T cell responses to antigenic peptides targeted to B cell surface Ig, Ia, or class I molecules. J. Exp. Med. 168:171.
12. Mjaaland, S. and Fossum, S. 1991. Antigen targeting with monoclonal antibodies as vectors-II. Further evidence that conjugation of antigen to specific monoclonal antibodies enhances uptake by antigen presenting cells. Int. Immunol. 3:1315.
13. Nabavi, N., Freeman, G. J., Gault, A., Godfrey, D., Nadler, L. M. and Glimcher, L. H. 1992. Signalling through the MHC class II cytoplasmic domain is required for antigen presentation and induces B7 expression. Nature 360:266.
14. Lane, P. J., McConnell, F. M., Schieven, G. L., Clark, E. A. and Ledbetter, J. A. 1990. The role of class II molecules in human B cell activation. Association with phosphatidyl inositol turnover, protein tyrosine phosphorylation, and proliferation. J. Immunol. 144:3684.
15. Carayanniotis, G., Skea, D. L., Luscher, M. A. and Barber, B. H. 1991. Adjuvant-independent immunization by immunotargeting antigens to MHC and non-MHC determinants in vivo. Mol. Immunol. 28:261.
16. Finkelman, F. D., Lees, A., Birnbaum, R., Gause, W. C. and Morris, S. C. 1996. Dendritic cells can present antigen in vivo in a tolerogenic or immunogenic fashion. J. Immunol. 157:1406.
17. White, A. L., Tutt, A. L., James, S. et al. 2010. Ligation of CD11c during vaccination promotes germinal centre induction and robust humoral responses without adjuvant. Immunology 131:141.
18. Miyake, K., Yamashita, Y., Ogata, M., Sudo, T. and Kimoto, M. 1995. RP105, a novel B cell surface molecule implicated in B cell activation, is a member of the leucine-rich repeat protein family. J. Immunol. 154:3333.
19. Nagai, Y., Shimazu, R., Ogata, H. et al. 2002. Requirement for MD-1 in cell surface expression of RP105/CD180 and B-cell responsiveness to lipopolysaccharide Blood 99:1699.
20. Yoon, S. I., Hong, M. and Wilson, I. A. 2011. An unusual dimeric structure and assembly for TLR4 regulator RP105-MD-1. Nat. Struct. Mol. Biol. 18:1028.
21. Otipoby, K. L., Nagai, Y., Shu, G. L., Miyake, K. and Clark, E. A. 2002. Leucocyte Typing VII. Oxford University Press, Harrogate, UK.
22. Valentine, M. A., Clark, E. A., Shu, G. L., Norris, N. A. and Ledbetter, J. A. 1988. Antibody to a novel 95-kDa surface glycoprotein on human B cells induces calcium mobilization and B cell activation. J. Immunol. 140:4071.
23. Miura, Y., Shimazu, R., Miyake, K. et al. 1998. RP105 is associated with MD-1 and transmits an activation signal in human B cells. Blood 92:2815.
24. Chaplin, J. W., Kasahara, S., Clark, E. A. and Ledbetter, J. A. 2011. Anti-CD180 (RP105) activates B cells to rapidly produce polyclonal Ig via a T cell and MyD88-independent pathway. J. Immunol. 187:4199.
25. Chaplin, J. W., Chappell, C. P. and Clark, E. A. 2013. Targeting antigens to CD180 rapidly induces antigen-specific IgG, affinity maturation, and immunological memory. J. Exp. Med. 210:2135.
26. Macauley, M. S., Pfrengle, F., Rademacher, C. et al. 2013. Antigenic liposomes displaying CD22 ligands induce antigenspecific B cell apoptosis. J. Clin. Invest. 123:3074.
27. Castro, F. V., Tutt, A. L., White, A. L. et al. 2008. CD11c provides an effective immunotarget for the generation of both CD4 and CD8 T cell responses. Eur. J. Immunol. 38:2263.
28. Postigo, A. A., Corbí, A. L., Sánchez-Madrid, F. and de Landázuri, M. O. 1991. Regulated expression and function of CD11c/CD18 integrin on human B lymphocytes. Relation between attachment to fibrinogen and triggering of proliferation through CD11c/CD18. J. Exp. Med. 174:1313.
29. Craxton, A., Magaletti, D., Ryan, E. J. and Clark, E. A. 2003. Macrophage-and dendritic cell-dependent regulation of human B-cell proliferation requires the TNF family ligand BAFF. Blood 101:4464.
30. Dubois, B., Massacrier, C., Vanbervliet, B. et al. 1998. Critical role of IL-12 in dendritic cell-induced differentiation of naive B lymphocytes. J. Immunol. 161:2223.
31. Fayette, J., Durand, I., Bridon, J. M. et al. 1998. Dendritic cells enhance the differentiation of naïve B cells into plasma cells in vitro. Scand. J. Immunol. 48:563.
32. Litinskiy, M. B., Nardelli, B., Hilbert, D. M. et al. 2002. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat. Immunol. 3:822.
33. Lahoud, M. H., Proietto, A. I., Ahmet, F. et al. 2009. The C-type lectin Clec12A present on mouse and human dendritic cells can serve as a target for antigen delivery and enhancement of antibody responses. J. Immunol. 182:7587.
34. Carter, R. W., Thompson, C., Reid, D. M., Wong, S. Y. and Tough, D. F. 2006. Preferential induction of CD4+ T cell responses through in vivo targeting of antigen to dendritic cell-associated C-type lectin-1. J. Immunol. 177:2276.
35. Caminschi, I., Proietto, A. I., Ahmet, F. et al. 2008. The dendritic cell subtype-restricted C-type lectin Clec9A is a target for vaccine enhancement. Blood 112:3264.
36. Corbett, A. J., Caminschi, I., McKenzie, B. S. et al. 2005. Antigen delivery via two molecules on the CD8-dendritic cell subset induces humoral immunity in the absence of conventional "danger". Eur. J. Immunol. 35:2815.
37. Kaden, S. A., Kurig, S., Vasters, K. et al. 2009. Enhanced dendritic cell-induced immune responses mediated by the novel C-type lectin receptor mDCAR1. J. Immunol. 183:5069.
38. Snider, D. P., Kaubisch, A. and Segal, D. M. 1990. Enhanced antigen immunogenicity induced by bispecific antibodies. J. Exp. Med. 171:1957.
39. Dudziak, D., Kamphorst, A. O., Heidkamp, G. F. et al. 2007. Differential antigen processing by dendritic cell subsets in vivo. Science 315:107.
40. Jiang, W., Swiggard, W. J., Heufler, C. et al. 1995. The receptor DEC-205 expressed by dendritic cells and thymic epithelial cells is involved in antigen processing. Nature 375:151.
41. Caminschi, I., Vremec, D., Ahmet, F. et al. 2012. Antibody responses initiated by Clec9A-bearing dendritic cells in normal and Batf3(-/-) mice. Mol. Immunol. 50:9.
42. Pajak, B., Garze, V., Davies, G., Bauer, J., Moser, M. and Chiavaroli, C. 2003. The adjuvant OM-174 induces both the migration and maturation of murine dendritic cells in vivo. Vaccine 21:836.
43. Boscardin, S. B., Hafalla, J. C., Masilamani, R. F. et al. 2006. Antigen targeting to dendritic cells elicits long-lived T cell help for antibody responses. J. Exp. Med. 203:599.
44. Lahoud, M. H., Ahmet, F., Kitsoulis, S. et al. 2011. Targeting antigen to mouse dendritic cells via Clec9A induces potent CD4 T cell responses biased toward a follicular helper phenotype. J. Immunol. 187:842.
45. Crotty, S. 2011. Follicular helper CD4 T cells (TFH). Annu. Rev. Immunol. 29:621.
46. Pooley, J. L., Heath, W. R. and Shortman, K. 2001. Cutting edge: intravenous soluble antigen is presented to CD4 T cells by CD8-dendritic cells, but cross-presented to CD8 T cells by CD8+ dendritic cells. J. Immunol. 166:5327.
47. den Haan, J. M., Lehar, S. M. and Bevan, M. J. 2000. CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J. Exp. Med. 192:1685.
48. Dresch, C., Ackermann, M., Vogt, B., de Andrade Pereira, B., Shortman, K. and Fraefel, C. 2011. Thymic but not splenic CD8+ DCs can efficiently cross-prime T cells in the absence of licensing factors. Eur. J. Immunol. 41:2544.
49. Chatterjee, B., Smed-Sörensen, A., Cohn, L. et al. 2012. Internalization and endosomal degradation of receptor-bound antigens regulate the efficiency of cross presentation by human dendritic cells. Blood 120:2011.
50. Kamphorst, A. O., Guermonprez, P., Dudziak, D. and Nussenzweig, M. C. 2010. Route of antigen uptake differentially impacts presentation by dendritic cells and activated monocytes. J. Immunol. 185:3426.
51. Cohn, L., Chatterjee, B., Esselborn, F. et al. 2013. Antigen delivery to early endosomes eliminates the superiority of human blood BDCA3+ dendritic cells at cross presentation. J. Exp. Med. 210:1049.
52. Joffre, O. P., Sancho, D., Zelenay, S., Keller, A. M. and Reise Sousa, C. 2010. Efficient and versatile manipulation of the peripheral CD4+ T-cell compartment by antigen targeting to DNGR-1/CLEC9A. Eur. J. Immunol. 40:1255.
53. Clark, M. R., Massenburg, D., Siemasko, K., Hou, P. and Zhang, M. 2004. B-cell antigen receptor signaling requirements for targeting antigen to the MHC class II presentation pathway. Curr. Opin. Immunol. 16:382.
54. Burgdorf, S., Kautz, A., Böhnert, V., Knolle, P. A. and Kurts, C. 2007. Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science 316:612.
55. Gilliet, M., Cao, W. and Liu, Y. J. 2008. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat. Rev. Immunol. 8:594.
56. Villadangos, J. A. and Young, L. 2008. Antigen-presentation properties of plasmacytoid dendritic cells. Immunity 29:352.
57. Loschko, J. and Krug, A. 2012. Antigen delivery to plasmacytoid dendritic cells-induction of tolerance and immunity. Crit. Rev. Immunol. 32:489.
58. Yu, C. F., Peng, W. M., Oldenburg, J. et al. 2010. Human plasmacytoid dendritic cells support Th17 cell effector function in response to TLR7 ligation. J. Immunol. 184:1159.
59. Matta, B. M., Castellaneta, A. and Thomson, A. W. 2010. Tolerogenic plasmacytoid DC. Eur. J. Immunol. 40:2667.
60. Takagi, H., Fukaya, T., Eizumi, K. et al. 2011. Plasmacytoid dendritic cells are crucial for the initiation of inflammation and T cell immunity in vivo. Immunity 35:958.
61. Boonstra, A., Asselin-Paturel, C., Gilliet, M. et al. 2003. Flexibility of mouse classical and plasmacytoid-derived dendritic cells in directing T helper type 1 and 2 cell development: dependency on antigen dose and differential toll-like receptor ligation. J. Exp. Med. 197:101.
62. Young, L. J., Wilson, N. S., Schnorrer, P. et al. 2008. Differential MHC class II synthesis and ubiquitination confers distinct antigen-presenting properties on conventional and plasmacytoid dendritic cells. Nat. Immunol. 9:1244.
63. Dzionek, A., Sohma, Y., Nagafune, J. et al. 2001. BDCA-2, a novel plasmacytoid dendritic cell-specific type II C-type lectin, mediates antigen capture and is a potent inhibitor of interferon alpha/beta induction. J. Exp. Med. 194:1823.
64. Meyer-Wentrup, F., Benitez-Ribas, D., Tacken, P. J. et al. 2008. Targeting DCIR on human plasmacytoid dendritic cells results in antigen presentation and inhibits IFN-alpha production. Blood 111:4245.
65. Loschko, J., Schlitzer, A., Dudziak, D. et al. 2011. Antigen delivery to plasmacytoid dendritic cells via BST2 induces protective T cellmediated immunity. J. Immunol. 186:6718.
66. Loschko, J., Heink, S., Hackl, D. et al. 2011. Antigen targeting to plasmacytoid dendritic cells via Siglec-H inhibits Th cell-dependent autoimmunity. J. Immunol. 187:6346.
67. Benitez-Ribas, D., Adema, G. J., Winkels, G. et al. 2006. Plasmacytoid dendritic cells of melanoma patients present exogenous proteins to CD4+ T cells after Fc gamma RII-mediated uptake. J. Exp. Med. 203:1629.
68. Moffat, J. M., Segura, E., Khoury, G. et al. 2013. Targeting antigen to bone marrow stromal cell-2 expressed by conventional and plasmacytoid dendritic cells elicits efficient antigen presentation. Eur. J. Immunol. 43:595.
69. Giordano, D., Li, C., Suthar, M. S. et al. 2011. Nitric oxide controls an inflammatory-like Ly6C(hi)PDCA1+ DC subset that regulates Th1 immune responses. J. Leukoc. Biol. 89:443.
70. Blasius, A. L., Cella, M., Maldonado, J., Takai, T. and Colonna, M. 2006. Siglec-H is an IPC-specific receptor that modulates type I IFN secretion through DAP12. Blood 107:2474.
71. Zhang, J., Raper, A., Sugita, N. et al. 2006. Characterization of Siglec-H as a novel endocytic receptor expressed on murine plasmacytoid dendritic cell precursors. Blood 107:3600.
72. Jaehn, P. S., Zaenker, K. S., Schmitz, J. and Dzionek, A. 2008. Functional dichotomy of plasmacytoid dendritic cells: antigenspecific activation of T cells versus production of type I interferon. Eur. J. Immunol. 38:1822.
73. Swiecki, M., Wang, Y., Gilfillan, S., Lenschow, D. J. and Colonna, M. 2012. Cutting edge: paradoxical roles of BST2/tetherin in promoting type I IFN response and viral infection. J. Immunol. 188:2488.
74. Riboldi, E., Daniele, R., Parola, C. et al. 2011. Human C-type lectin domain family 4, member C (CLEC4C/BDCA-2/CD303) is a receptor for asialo-galactosyl-oligosaccharides. J. Biol. Chem. 286:35329.
75. Cao, W., Zhang, L., Rosen, D. B. et al. 2007. BDCA2/Fc epsilon RI gamma complex signals through a novel BCR-like pathway in human plasmacytoid dendritic cells. PLoS Biol. 5:e248.
76. Bao, M. and Liu, Y. J. 2013. Regulation of TLR7/9 signaling in plasmacytoid dendritic cells. Protein Cell 4:40.
77. Kasahara, S. and Clark, E. A. 2012. Dendritic cell-associated lectin 2 (DCAL2) defines a distinct CD8a-dendritic cell subset. J. Leukoc. Biol. 91:437.