Antigen delivery via two molecules on the CD8- dendritic cell subset induces humoral immunity in the absence of conventional "danger"

European Journal of Immunology

Volumn 35, Issue 10, 2005, Pages 2815-2825

  Corbett, Alexandra J ^a,b,d   Caminschi, Irina ^a   McKenzie, Brent S ^a   Brady, Jamie L ^a   Wright, Mark D ^c   Mottram, Patricia L ^c   Hogarth, P Mark ^c   Hodder, Anthony N ^a   Zhan, Yifan ^a   Tarlinton, David M ^a   Shortman, Ken ^a   Lew, Andrew M ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b Department of Civil and Environmental Engineering   (Australia)

^c AUSTIN RESEARCH INSTITUTE   (Australia)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Ab response; Danger; DC subset; Fc; Targeting

Indexed keywords

FC RECEPTOR; LECTIN RECEPTOR; MONOCLONAL ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIGEN FUNCTION; ANTIGEN PRESENTATION; ARTICLE; CELL FUNCTION; COMPLEMENT FIXATION; CONTROLLED STUDY; CPG ISLAND; DENDRITIC CELL; FEMALE; HUMORAL IMMUNITY; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOSTIMULATION; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; STEADY STATE; T LYMPHOCYTE;

ANIMALS; ANTIBODY FORMATION; ANTIGEN PRESENTATION; ANTIGENS, CD; ANTIGENS, CD8; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPIDERMAL GROWTH FACTOR; FEMALE; LECTINS, C-TYPE; MICE; RECEPTORS, CELL SURFACE;

EID: 27644563834     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200526100     Document Type: Article

References (51)

1. Shortman, K. and Liu, Y. J., Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2002. 2: 151-161.
2. Steinman, R. M., Hawiger, D. and Nussenzweig, M. C., Tolerogenic dendritic cells. Annu. Rev. Immunol. 2003. 21: 685-711.
3. - dendritic cells in the induction of primary immune responses in vivo. J. Leukoc. Biol. 1999. 66: 242-246.
4. Pulendran, B., Smith, J. L., Caspary, G., Brasel, K., Pettit, D., Maraskovsky, E. and Maliszewski, C. R., Distinct dendritic cell subsets differentially regulate the class of immune response in vivo. Proc. Natl. Acad. Sci. USA 1999. 96: 1036-1041.
5. 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.
6. Pooley, J. L., Heath, W. R. and Shortman, K., 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. 2001. 166: 5327-5330.
7. Smith, C. M., Belz, G. T., Wilson, N. S., Villadangos, J. A., Shortman, K., Carbone, F. R. and Heath, W. R., Cutting edge: conventional CD8alpha(+) dendritic cells are preferentially involved in CTL priming after footpad infection with herpes simplex virus-1. J. Immunol. 2003. 170: 4437-4440.
8. Kronin, V., Fitzmaurice, C. J., Caminschi, I., Shortman, K., Jackson, D. C. and Brown, L. E., Differential effect of CD8(+) and CD8 (-) dendritic cells in the stimulation of secondary CD4(+) T cells. Int. Immunol. 2001. 13: 465-473.
9. Iyoda, T., Shimoyama, S., Liu, K., Omatsu, Y., Akiyama, Y., Maeda, Y., Takahara, K. et al., The CD8(+) dendritic cell subset selectively endocytoses dying cells in culture and in vivo. J. Exp. Med. 2002. 195: 1289-1302.
10. Caminschi, I., Lucas, K. M., O'Keeffe, M. A., Hochrein, H., Laabi, Y., Kontgen, F., Lew, A. M. et al., Molecular cloning of F4/80-like-receptor, a seven-span membrane protein expressed differentially by dendritic cell and monocyte-macrophage subpopulations. J. Immunol. 2001. 167: 3570-3576.
11. Caminschi, I., Lucas, K. M., O'Keeffe, M. A., Hochrein, H., Laabi, Y., Brodnicki, T. C., Lew, A. M. et al., Molecular cloning of a C-type lectin superfamily protein differentially expressed by CD8alpha(-) splenic dendritic cells. Mol. Immunol. 2001. 38: 365-373.
12. Engering, A., Geijtenbeek, T. B., van Vliet, S. J., Wijers, M., van Liempt, E., Demaurex, N., Lanzavecchia, A. et al., The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J. Immunol. 2002. 168: 2118-2126.
13. Curtis, B. M., Scharnowske, S. and Watson, A. J., Sequence and expression of a membrane-associated C-type lectin that exhibits CD4-independent binding of human immunodeficiency virus envelope glycoprotein gp120. Proc. Natl. Acad. Sci. USA 1992. 89: 8356-8360.
14. Geijtenbeek, T. B., Van Vliet, S. J., Koppel, E. A., Sanchez-Hernandez, M., Vandenbroucke-Grauls, C. M., Appelmelk, B. and Van Kooyk, Y., Mycobacteria target DC-SIGN to suppress dendritic cell function. J. Exp. Med. 2003. 197: 7 17.
15. Jiang, W., Swiggard, W. J., Heufler, C., Peng, M., Mirza, A., Steinman, R. M. and Nussenzweig, M. C., The receptor DEC-205 expressed by dendritic cells and thymic epithelial cells is involved in antigen processing. Nature 1995. 375: 151-155.
16. Vremec, D. and Shortman, K., Dendritic cell subtypes in mouse lymphoid organs: cross-correlation of surface markers, changes with incubation, and differences among thymus, spleen, and lymph nodes. J. Immunol. 1997. 159: 565-573.
17. McLellan, A. D., Kapp, M., Eggert, A., Linden, C., Bommhardt, U., Brocker, E.-B., Kammerer, U. and Kampgen, E., Anatomic location and T-cell stimulatory functions ofmouse dendritic cell subsets defined by CD4 and CD8 expression. Blood 2002. 99: 2084-2093.
18. Hawiger, D., Inaba, K., Dorsett, Y., Guo, M., Mahnke, K., Rivera, M., Ravetch, J. V. et al., Dendritic cells induce peripheral t cell unresponsiveness under steady state conditions in vivo. J. Exp. Med. 2001. 194: 769-780.
19. + T cell tolerance. J. Exp. Med. 2002. 196: 1627-1638.
20. Suss, G. and Shortman, K., A subclass of dendritic cells kills CD4 T cells via Fas/Fas-ligand- induced apoptosis. J. Exp. Med. 1996. 183: 1789-1796.
21. de St Groth, B. F., The evolution of self-tolerance: a new cell arises to meet the challenge of self-reactivity. Immunol. Today 1998. 19: 448-454.
22. Steinman, R. M., Turley, S., Mellman, I. and Inaba, K., The induction of tolerance by dendritic cells that have captured apoptotic cells. J. Exp. Med. 2000. 191: 411-416.
23. O'Keeffe, M., Hochrein, H., Vremec, D., Caminschi, I., Miller, J. L., Anders, E. M., Wu, L. et al., Mouse plasmacytoid cells: long-lived cells, heterogeneous in surface phenotype and function, that differentiate into CD8(+) dendritic cells only after microbial stimulus. J. Exp. Med. 2002. 196: 1307-1319.
24. Carayanniotis, G. and Barber, B. H., Adjuvant-free IgG responses induced with antigen coupled to antibodies against class II MHC. Nature 1987. 327: 59-61.
25. Lunde, E., Western, K. H., Rasmussen, I. B., Sandlie, I. and Bogen, B., Efficient delivery of T cell epitopes to APC by use of MHC class II-specific Troybodies. J. Immunol. 2002. 168: 2154-2162.
26. Wang, H., Griffiths, M. N., Burton, D. R. and Ghazal, P., Rapid antibody responses by low-dose, single-step, dendritic cell- targeted immunization. Proc. Natl. Acad. Sci. USA 2000. 97: 847-852.
27. Boyle, J. S., Brady, J. L. and Lew, A. M., Enhanced responses to a DNA vaccine encoding a fusion antigen that is directed to sites of immune induction. Nature 1998. 392: 408-411.
28. Finkelman, F. D., Lees, A., Birnbaum, R., Gause, W. C. and Morris, S. C., Dendritic cells can present antigen in vivo in a tolerogenic or immunogenic fashion. J. Immunol. 1996. 157: 1406-1414.
29. Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., Matsumoto, M. et al., A Toll-like receptor recognizes bacterial DNA. Nature 2000. 408: 740-745.
30. Takai, T., Li, M., Sylvestre, D., Clynes, R. and Ravetch, J. V., FcR gamma chain deletion results in pleiotrophic effector cell defects. Cell 1994. 76: 519-529.
31. Woof, J. M., Fc receptors and their interaction with antibodies. Biochem. Soc. Trans. 1990. 18: 217-218.
32. Bruggemann, M., Teale, C., Clark, M., Bindon, C. and Waldmann, H., A matched set of rat/mouse chimeric antibodies. Identification and biological properties of rat H chain constant regions mu, gamma 1, gamma 2a, gamma 2b, gamma 2c, epsilon, and alpha. J. Immunol. 1989. 142: 3145-3150.
33. Kawabata, S., Terao, Y., Fujiwara, T., Nakagawa, I. and Hamada, S., Targeted salivary gland immunization with plasmid DNA elicits specific salivary immunoglobulin A and G antibodies and serum immunoglobulin G antibodies in mice. Infect. Immun. 1999. 67: 5863-5868.
34. Boyle, J. S., Barr, I. G. and Lew, A. M., Strategies for improving responses to DNA vaccines. Mol. Med. 1999. 5: 1-8.
35. Maloy, K. J., Erdmann, I., Basch, V., Sierro, S., Kramps, T. A., Zinkernagel, R. M., Oehen, S. and Kundig, T. M., Intralymphatic immunization enhances DNA vaccination. Proc. Natl. Acad. Sci. USA 2001. 98: 3299-3303.
36. Nilsson, B. O., Svalander, P. C. and Larsson, A., Immunization of mice and rabbits by intrasplenic deposition of nanogram quantities of protein attached to Sepharose beads or nitrocellulose paper strips. J. Immunol. Methods 1987. 99: 67-75.
37. Sigel, M. B., Sinha, Y. N. and VanderLaan, W. P., Production of antibodies by inoculation into lymph nodes. Methods Enzymol. 1983. 93: 3-12.
38. Bonifaz, L., Bonnyay, D., Charalambous, A., Darguste, D. I., Fujii, S.-I., Soares, H., Brimnes, M. K. et al., In vivo targeting of antigens to maturing dendritic cells via the DEC-205 receptoer improves T cell vaccination. J. Exp. Med. 2004. 199: 815-824.
39. + T-helper cells by induction of FAS-independent T-cell apoptosis. Immunology 2003. 109: 32-40.
40. Liu, Y. J., Kanzler, H., Soumelis, V. and Gilliet, M., Dendritic cell lineage, plasticity and cross-regulation. Nat. Immunol. 2001. 2: 585-589.
41. Grohmann, U., Bianchi, R., Orabona, C., Fallarino, F., Vacca, C., Micheletti, A., Fioretti, M. C. and Puccetti, P., Functional plasticity of dendritic cell subsets as mediated by CD40 versus B7 activation. J. Immunol. 2003. 171: 2581-2587.
42. 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.
43. Kronin, V., Wu, L., Gong, S., Nussenzweig, M. C. and Shortman, K., DEC-205 as a marker of dendritic cells with regulatory effects on CD8 T cell responses. Int. Immunol. 2000. 12: 731-735.
44. Manoj, S., Griebel, P. J., Babiuk, L. A. and van Drunen Littel-van den Hark, S., Targeting with bovine CD154 enhances humoral immune responses induced by a DNA vaccine in sheep. J. Immunol. 2003. 170: 989-996.
45. Krieg, A. M., Yi, A. K., Matson, S., Waldschmidt, T. J., Bishop, G. A., Teasdale, R., Koretzky, G. A. and Klinman, D. M., CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 1995. 374: 546-549.
46. McKenzie, B. S., Corbett, A. J., Johnson, S., Brady, J. L., Pleasance, J., Kramer, D. R., Boyle, J. S. et al., Bypassing luminal barriers, delivery to a gut addressin by parenteral targeting elicits local IgA responses. Int. Immunol. 2004. 16: 1613-1622.
47. Boyle, J. S., Koniaras, C. and Lew, A. M., Influence of cellular location of expressed antigen on the efficacy of DNA vaccination: cytotoxic T lymphocyte and antibody responses are suboptimal when antigen is cytoplasmic after intramuscular DNA immunization. Int. Immunol. 1997. 9: 1897-1906.
48. Hunter, R., Standardization of the chloramine-T method of protein iodination. Proc. Soc. Exp. Biol. Med. 1970. 133: 989-992.
49. Vremec, D., Pooley, J., Hochrein, H., Wu, L. and Shortman, K., CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J. Immunol. 2000. 164: 2978-2986.
50. Zhan, Y., Brady, J. L., Sutherland, R. M. and Lew, A. M., Without CD4 help, CD8 rejection of pig xenografts requires CD28 costimulation but not perforin killing. J. Immunol. 2001. 167: 6279-6285.
51. Xu, Y., Beavitt, S. J., Harder, K. W., Hibbs, M. L. and Tarlinton, D. M., The activation and subsequent regulatory roles of Lyn and CD19 after B cell receptor ligation are independent. J. Immunol. 2002. 169: 6910-6918.