Antigen delivery to CD11c+CD8- dendritic cells induces protective immune responses against experimental melanoma in mice in vivo

Journal of Immunology

Volumn 192, Issue 12, 2014, Pages 5830-5838

  Neubert, Kirsten ^a   Lehmann, Christian H K ^a   Heger, Lukas ^a   Baranska, Anna ^a   Staedtler, Anna Maria ^a   Buchholz, Veit R ^b   Yamazaki, Sayuri ^c   Heidkamp, Gordon F ^a   Eissing, Nathalie ^a   Zebroski, Henry ^d   Nussenzweig, Michel C ^d   Nimmerjahn, Falk ^e   Dudziak, Diana ^a  

^a UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c NAGOYA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCES   (Japan)

^d ROCKEFELLER UNIVERSITY   (United States)

^e UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 LIGAND MONOCLONAL ANTIBODY; CD8 ANTIGEN; CELL ANTIBODY; DEC205 ANTIBODY; DENDRITIC CELL INHIBITORY RECEPTOR 2 ANTIBODY; GAMMA INTERFERON; GLYCOPROTEIN P 15095; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2A ANTIBODY; IMMUNOGLOBULIN G2B ANTIBODY; IMMUNOGLOBULIN G2C ANTIBODY; IMMUNOGLOBULIN G3 ANTIBODY; INTERLEUKIN 4; POLYINOSINIC POLYCYTIDYLIC ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ANTIBODY TITER; ARTICLE; CANCER IMMUNIZATION; CANCER SURVIVAL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL SUBPOPULATION; CELLULAR IMMUNITY; COMPARATIVE STUDY; CONTROLLED STUDY; CROSS PRESENTATION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; DRUG TARGETING; EXPERIMENTAL MELANOMA; FEMALE; HEK293 CELL LINE; HUMORAL IMMUNITY; IMMUNOMODULATION; IMMUNOSTIMULATION; IN VIVO STUDY; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; SURVIVAL RATE; TH1 TH2 BALANCE; TUMOR IMMUNITY; TUMOR VOLUME;

ANIMALS; ANTIBODIES; ANTIGEN PRESENTATION; ANTIGENS, CD11C; ANTIGENS, CD8; ANTIGENS, NEOPLASM; CELL LINE, TUMOR; DENDRITIC CELLS; INTERFERON INDUCERS; MALE; MELANOMA; MICE; NEOPLASMS, EXPERIMENTAL; POLY I-C; TOLL-LIKE RECEPTOR 3;

EID: 84902173181     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300975     Document Type: Article

References (57)

1. Miller, A. J., and M. C. Mihm, Jr. 2006. Melanoma. N. Engl. J. Med. 355:51-65.
2. Ashman, L. K. 1987. The immunogenicity of tumour cells. Immunol. Cell Biol. 65:271-277.
3. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392:245-252.
4. Aarntzen, E. H., G. Schreibelt, K. Bol, W. J. Lesterhuis, A. J. Croockewit, J. H. De Wilt, M. M. Van Rossum, W. A. Blokx, J. F. Jacobs, T. Duiveman-de Boer, et al. 2012. Vaccination with mRNA-electroporated dendritic cells induces robust tumor antigen-specific CD4+ and CD8+ T cells responses in stage III and IV melanoma patients. Clin. Cancer Res. 18:5460-5470.
5. Kreutz, M., B. Giquel, Q. Hu, R. Abuknesha, S. Uematsu, S. Akira, F. O. Nestle, and S. S. Diebold. 2012. Antibody-antigen-adjuvant conjugates enable codelivery of antigen and adjuvant to dendritic cells in cis but only have partial targeting specificity. PLoS ONE 7:e40208.
6. Tacken, P. J., I. J. De Vries, R. Torensma, and C. G. Figdor. 2007. Dendritic-cell immunotherapy: from ex vivo loading to in vivo targeting. Nat. Rev. Immunol. 7:790-802.
7. Van Duin, D., R. Medzhitov, and A. C. Shaw. 2006. Triggering TLR signaling in vaccination. Trends Immunol. 27:49-55.
8. Steinman, R. M., and J. Banchereau. 2007. Taking dendritic cells into medicine. Nature 449:419-426.
9. Liu, K., and M. C. Nussenzweig. 2010. Origin and development of dendritic cells. Immunol. Rev. 234:45-54.
10. Shortman, K., and W. R. Heath. 2010. The CD8+ dendritic cell subset. Immunol. Rev. 234:18-31.
11. Shortman, K., and S. H. Naik. 2007. Steady-state and inflammatory dendriticcell development. Nat. Rev. Immunol. 7:19-30.
12. Villadangos, J. A., and P. Schnorrer. 2007. Intrinsic and cooperative antigenpresenting functions of dendritic-cell subsets in vivo. Nat. Rev. Immunol. 7:543-555.
13. Bonifaz, L., D. Bonnyay, K. Mahnke, M. Rivera, M. C. Nussenzweig, and R. M. Steinman. 2002. Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance. J. Exp. Med. 196:1627-1638.
14. Den Haan, J. M., and M. J. Bevan. 2002. Constitutive versus activation-dependent cross-presentation of immune complexes by CD8 (+) and CD8 (2) dendritic cells in vivo. J. Exp. Med. 196:817-827.
15. Dudziak, D., A. O. Kamphorst, G. F. Heidkamp, V. R. Buchholz, C. Trumpfheller, S. Yamazaki, C. Cheong, K. Liu, H. W. Lee, C. G. Park, et al. 2007. Differential antigen processing by dendritic cell subsets in vivo. Science 315:107-111.
16. Figdor, C. G., Y. Van Kooyk, and G. J. Adema. 2002. C-type lectin receptors on dendritic cells and Langerhans cells. Nat. Rev. Immunol. 2:77-84.
17. Pooley, J. L., W. R. Heath, and K. Shortman. 2001. Cutting edge: intravenous soluble antigen is presented to CD4 T cells by CD82 dendritic cells, but crosspresented to CD8 T cells by CD8+ dendritic cells. J. Immunol. 166:5327-5330.
18. Schnorrer, P., G. M. Behrens, N. S. Wilson, J. L. Pooley, C. M. Smith, D. El-Sukkari, G. Davey, F. Kupresanin, M. Li, E. Maraskovsky, et al. 2006. The dominant role of CD8+ dendritic cells in cross-presentation is not dictated by antigen capture. Proc. Natl. Acad. Sci. USA 103:10729-10734.
19. Soares, H., H. Waechter, N. Glaichenhaus, E. Mougneau, H. Yagita, O. Mizenina, D. Dudziak, M. C. Nussenzweig, and R. M. Steinman. 2007. A subset of dendritic cells induces CD4+ T cells to produce IFN-gamma by an IL-12-independent but CD70-dependent mechanism in vivo. J. Exp. Med. 204:1095-1106.
20. Kawai, T., and S. Akira. 2011. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34:637-650.
21. Hawiger, D., K. Inaba, Y. Dorsett, M. Guo, K. Mahnke, M. Rivera, J. V. Ravetch, R. M. Steinman, and M. C. Nussenzweig. 2001. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J. Exp. Med. 194:769-779.
22. Geijtenbeek, T. B., and S. I. Gringhuis. 2009. Signalling through C-type lectin receptors: shaping immune responses. Nat. Rev. Immunol. 9:465-479.
23. Sancho, D., D. Mourão-Sá, O. P. Joffre, O. Schulz, N. C. Rogers, D. J. Pennington, J. R. Carlyle, and C. Reis E Sousa. 2008. Tumor therapy in mice via antigen targeting to a novel, DC-restricted C-type lectin. J. Clin. Invest. 118:2098-2110.
24. Bozzacco, L., C. Trumpfheller, Y. Huang, M. P. Longhi, I. Shimeliovich, J. D. Schauer, C. G. Park, and R. M. Steinman. 2010. HIV gag protein is efficiently cross-presented when targeted with an antibody towards the DEC-205 receptor in Flt3 ligand-mobilized murine DC. Eur. J. Immunol. 40:36-46.
25. Do, Y., A. M. Didierlaurent, S. Ryu, H. Koh, C. G. Park, S. Park, D. S. Perlin, B. S. Powell, and R. M. Steinman. 2012. Induction of pulmonary mucosal immune responses with a protein vaccine targeted to the DEC-205/CD205 receptor. Vaccine 30:6359-6367.
26. Do, Y., H. Koh, C. G. Park, D. Dudziak, P. Seo, S. Mehandru, J. H. Choi, C. Cheong, S. Park, D. S. Perlin, et al. 2010. Targeting of LcrV virulence protein from Yersinia pestis to dendritic cells protects mice against pneumonic plague. Eur. J. Immunol. 40:2791-2796.
27. Idoyaga, J., A. Lubkin, C. Fiorese, M. H. Lahoud, I. Caminschi, Y. Huang, A. Rodriguez, B. E. Clausen, C. G. Park, C. Trumpfheller, and R. M. Steinman. 2011. Comparable T helper 1 (Th1) and CD8 T-cell immunity by targeting HIV gag p24 to CD8 dendritic cells within antibodies to Langerin, DEC205, and Clec9A. Proc. Natl. Acad. Sci. USA 108:2384-2389.
28. Charalambous, A., M. Oks, G. Nchinda, S. Yamazaki, and R. M. Steinman. 2006. Dendritic cell targeting of survivin protein in a xenogeneic form elicits strong CD4+ T cell immunity to mouse survivin. J. Immunol. 177:8410-8421.
29. Wang, B., N. Zaidi, L. Z. He, L. Zhang, J. M. Kuroiwa, T. Keler, and R. M. Steinman. 2012. Targeting of the non-mutated tumor antigen HER2/neu to mature dendritic cells induces an integrated immune response that protects against breast cancer in mice. Breast Cancer Res. 14:R39.
30. Bonifaz, L. C., D. P. Bonnyay, A. Charalambous, D. I. Darguste, S. Fujii, H. Soares, M. K. Brimnes, B. Moltedo, T. M. Moran, and R. M. Steinman. 2004. In vivo targeting of antigens to maturing dendritic cells via the DEC-205 receptor improves T cell vaccination. J. Exp. Med. 199:815-824.
31. Mahnke, K., Y. Qian, S. Fondel, J. Brueck, C. Becker, and A. H. Enk. 2005. Targeting of antigens to activated dendritic cells in vivo cures metastatic melanoma in mice. Cancer Res. 65:7007-7012.
32. Huleatt, J. W., and L. Lefrançois. 1995. Antigen-driven induction of CD11c on intestinal intraepithelial lymphocytes and CD8+ T cells in vivo. J. Immunol. 154:5684-5693.
33. Lin, Y., T. J. Roberts, V. Sriram, S. Cho, and R. R. Brutkiewicz. 2003. Myeloid marker expression on antiviral CD8+ T cells following an acute virus infection. Eur. J. Immunol. 33:2736-2743.
34. Laouar, Y., F. S. Sutterwala, L. Gorelik, and R. A. Flavell. 2005. Transforming growth factor-beta controls T helper type 1 cell development through regulation of natural killer cell interferon-gamma. Nat. Immunol. 6:600-607.
35. Probst, H. C., K. Tschannen, B. Odermatt, R. Schwendener, R. M. Zinkernagel, and M. Van Den Broek. 2005. Histological analysis of CD11c-DTR/GFP mice after in vivo depletion of dendritic cells. Clin. Exp. Immunol. 141:398-404.
36. Racine, R., M. Chatterjee, and G. M. Winslow. 2008. CD11c expression identifies a population of extrafollicular antigen-specific splenic plasmablasts responsible for CD4 T-independent antibody responses during intracellular bacterial infection. J. Immunol. 181:1375-1385.
37. Wei, H., S. Wang, D. Zhang, S. Hou, W. Qian, B. Li, H. Guo, G. Kou, J. He, H. Wang, and Y. Guo. 2009. Targeted delivery of tumor antigens to activated dendritic cells via CD11c molecules induces potent antitumor immunity in mice. Clin. Cancer Res. 15:4612-4621.
38. Falo, L. D., Jr., M. Kovacsovics-Bankowski, K. Thompson, and K. L. Rock. 1995. Targeting antigen into the phagocytic pathway in vivo induces protective tumour immunity. Nat. Med. 1:649-653.
39. Boscardin, S. B., J. C. Hafalla, R. F. Masilamani, A. O. Kamphorst, H. A. Zebroski, U. Rai, A. Morrot, F. Zavala, R. M. Steinman, R. S. Nussenzweig, and M. C. Nussenzweig. 2006. Antigen targeting to dendritic cells elicits long-lived T cell help for antibody responses. J. Exp. Med. 203:599-606.
40. Liu, S., R. Tobias, S. McClure, G. Styba, Q. Shi, and G. Jackowski. 1997. Removal of endotoxin from recombinant protein preparations. Clin. Biochem. 30:455-463.
41. Heidkamp, G. F., K. Neubert, E. Haertel, F. Nimmerjahn, M. C. Nussenzweig, and D. Dudziak. 2010. Efficient generation of a monoclonal antibody against the human C-type lectin receptor DCIR by targeting murine dendritic cells. Immunol. Lett. 132:69-78.
42. Reiner, S. L., and R. M. Locksley. 1995. The regulation of immunity to Leishmania major. Annu. Rev. Immunol. 13:151-177.
43. Trunova, G. V., O. V. Makarova, M. E. Diatroptov, I. M. Bogdanova, L. P. Mikchailova, and S. O. Abdulaeva. 2011. Morphofunctional characteristic of the immune system in BALB/c and C57BL/6 mice. Bull. Exp. Biol. Med. 151:99-102.
44. Stavnezer, J. 2000. Molecular processes that regulate class switching. Curr. Top. Microbiol. Immunol. 245:127-168.
45. Zhang, K. 2003. Accessibility control and machinery of immunoglobulin class switch recombination. J. Leukoc. Biol. 73:323-332.
46. Bonehill, A., A. M. Van Nuffel, J. Corthals, S. Tuyaerts, C. Heirman, V. François, D. Colau, P. Van Der Bruggen, B. Neyns, and K. Thielemans. 2009. Single-step antigen loading and activation of dendritic cells by mRNA electroporation for the purpose of therapeutic vaccination in melanoma patients. Clin. Cancer Res. 15:3366-3375.
47. Nestle, F. O., S. Alijagic, M. Gilliet, Y. Sun, S. Grabbe, R. Dummer, G. Burg, and D. Schadendorf. 1998. Vaccination of melanoma patients with peptide- or tumor lysate-pulsed dendritic cells. Nat. Med. 4:328-332.
48. Schuler, G. 2010. Dendritic cells in cancer immunotherapy. Eur. J. Immunol. 40:2123-2130.
49. Thurner, B., I. Haendle, C. Röder, D. Dieckmann, P. Keikavoussi, H. Jonuleit, A. Bender, C. Maczek, D. Schreiner, P. Von Den Driesch, et al. 1999. Vaccination with mage-3A1 peptide-pulsed mature, monocyte-derived dendritic cells expands specific cytotoxic T cells and induces regression of some metastases in advanced stage IV melanoma. J. Exp. Med. 190:1669-1678.
50. Van Nuffel, A. M., J. Corthals, B. Neyns, C. Heirman, K. Thielemans, and A. Bonehill. 2010. Immunotherapy of cancer with dendritic cells loaded with tumor antigens and activated through mRNA electroporation. Methods Mol. Biol. 629:405-452.
51. Tacken, P. J., and C. G. Figdor. 2011. Targeted antigen delivery and activation of dendritic cells in vivo: steps towards cost effective vaccines. Semin. Immunol. 23:12-20.
52. Steinman, R. M. 2012. Decisions about dendritic cells: past, present, and future. Annu. Rev. Immunol. 30:1-22.
53. Lahoud, M. H., F. Ahmet, S. Kitsoulis, S. S. Wan, D. Vremec, C. N. Lee, B. Phipson, W. Shi, G. K. Smyth, A. M. Lew, 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. 187:842-850.
54. Loschko, J., A. Schlitzer, D. Dudziak, I. Drexler, N. Sandholzer, C. Bourquin, W. Reindl, and A. B. Krug. 2011. Antigen delivery to plasmacytoid dendritic cells via BST2 induces protective T cell-mediated immunity. J. Immunol. 186:6718-6725.
55. Trumpfheller, C., J. S. Finke, C. B. López, T. M. Moran, B. Moltedo, H. Soares, Y. Huang, S. J. Schlesinger, C. G. Park, M. C. Nussenzweig, et al. 2006. Intensified and protective CD4+ T cell immunity in mice with anti-dendritic cell HIV gag fusion antibody vaccine. J. Exp. Med. 203:607-617.
56. Nimmerjahn, F., and J. V. Ravetch. 2005. Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science 310:1510-1512.
57. Hsieh, C. S., S. E. Macatonia, A. O'Garra, and K. M. Murphy. 1995. T cell genetic background determines default T helper phenotype development in vitro. J. Exp. Med. 181:713-721