HIV gag protein is efficiently cross-presented when targeted with an antibody towards the DEC-205 receptor in Flt3 ligand-mobilized murine DC

European Journal of Immunology

Volumn 40, Issue 1, 2010, Pages 36-46

  Bozzacco, Leonia ^a   Trumpfheller, Christine ^a   Huang, Yaoxing ^b   Longhi, Maria Paula ^a   Shimeliovich, Irina ^a   Schauer, Joseph D ^a   Park, Chae Gyu ^a   Steinman, Ralph M ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b AARON DIAMOND AIDS RESEARCH CENTER   (United States)

Author keywords

DC; FLt3L; Poly IC

Indexed keywords

ANTIGEN P24; CD135 ANTIGEN; DEC 205 RECEPTOR; FLT3 LIGAND; GAG PROTEIN; GLYCOPROTEIN P 15095; LYMPHOCYTE ANTIGEN RECEPTOR; UNCLASSIFIED DRUG; VIRUS PROTEIN; ANTIBODY; CELL SURFACE RECEPTOR; DEC-205 RECEPTOR; FLT3 LIGAND PROTEIN; LECTIN; LEUKOCYTE ANTIGEN; MEMBRANE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL FUNCTION; CONTROLLED STUDY; CROSS PRESENTATION; CYTOKINE RELEASE; DENDRITIC CELL; HUMAN IMMUNODEFICIENCY VIRUS; MELANOMA; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN TARGETING; SPLEEN CELL; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL LINE; CROSS REACTION; HAMSTER; IMMUNOLOGY;

ANIMALS; ANTIBODIES; ANTIGENS, CD; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; CRICETINAE; CROSS REACTIONS; DENDRITIC CELLS; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV; LECTINS, C-TYPE; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; RECEPTORS, CELL SURFACE;

EID: 74249124188     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200939748     Document Type: Article

References (60)

1. Heath, W. R., Belz, G. T., Behrens, G. M., Smith, C. M., Forehan, S. P., Parish, I. A., Davey, G. M., Cross-presentation, dendritic cell subsets, and the generation of immunity to cellular antigens. Immunol. Rev. 2004. 199: 9-26.
2. Regnault, A., Lankar, D., Lacabanne, V., Rodriguez, A., Thery, C., Rescigno, M., Saito, T. et al., Fcγ 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.
3. Kalergis, A. M. and Ravetch, J. V., Inducing tumor immunity through the selective engagement of activating Fcγ receptors on dendritic cells. J. Exp. Med. 2002. 195: 1653-1659.
4. Den Haan, J. M. and Bevan, M. J., Constitutive versus activationdependent cross-presentation of immune complexes by CD8(+) and CD8(-) dendritic cells in vivo. J. Exp. Med. 2002. 196: 817-827.
5. Liu, K., Iyoda, T., Saternus, M., Kimura, K., Inaba, K. and Steinman, R. M., Immune tolerance after delivery of dying cells to dendritic cells in situ. J. Exp. Med. 2002. 196: 1091-1097.
6. + dendritic cell subset selectively endocytoses dying cells in culture and in vivo. J. Exp. Med. 2002. 195: 1289-1302.
7. + T cell tolerance. J. Exp. Med. 2002. 196: 1627-1638.
8. Tacken, P. J., Joosten, B., Reddy, A., Wu, D., Eek, A., Laverman, P., Kretz-Rommel, A. et al., No advantage of cell-penetrating peptides over receptor-specific antibodies in targeting antigen to human dendritic cells for cross-presentation. J. Immunol. 2008. 180: 7687-7696.
9. Burgdorf, S., Lukacs-Kornek, V. and Kurts, C., The mannose receptor mediates uptake of soluble but not of cell-associated antigen for cross-presentation. J. Immunol. 2006. 176: 6770-6776.
10. Idoyaga, J., Cheong, C., Suda, K., Suda, N., Kim, J. Y., Lee, H., Park, C. G. and Steinman, R. M., Langerin/CD207 receptor on dendritic cells mediates efficient antigen presentation on MHC I and II products in vivo. J. Immunol. 2008. 180: 3647-3650.
11. Delneste, Y., Magistrelli, G., Gauchat, J., Haeuw, J., Aubry, J., Nakamura, K., Kawakami-Honda, N. et al., Involvement of LOX-1 in dendritic cell-mediated antigen cross-presentation. Immunity 2002. 17: 353-362.
12. Sancho, D., Mourao-Sa, D., Joffre, O. P., Schulz, O., Rogers, N. C., Pennington, D. J., Carlyle, J. R. and Reis, E. S. C., Tumor therapy in mice via antigen targeting to a novel, DC-restricted C-type lectin. J. Clin. Invest. 2008. 118: 2098-2110.
13. Choi, J. H., Do, Y., Cheong, C., Koh, H., Boscardin, S. B., Oh, Y. S., Bozzacco, L. et al., Identification of antigen-presenting dendritic cells in mouse aorta and cardiac valves. J. Exp. Med. 2009. 206: 497-505.
14. Boscardin, S. B., Hafalla, J. C., Masilamani, R. F., Kamphorst, A. O., Zebroski, H. A., Rai, U., Morrot, A. et al., Antigen targeting to dendritic cells elicits long-lived T cell help for antibody responses. J. Exp. Med. 2006. 203: 599-606.
15. Sponaas, A. M., Cadman, E. T., Voisine, C., Harrison, V., Boonstra, A., O'Garra, A. and Langhorne, J., Malaria infection changes the ability of splenic dendritic cell populations to stimulate antigen-specific T cells. J. Exp. Med. 2006. 203: 1427-1433.
16. Wilson, N. S., Behrens, G. M., Lundie, R. J., Smith, C. M., Waithman, J., Young, L., Forehan, S. P. et al., Systemic activation of dendritic cells by Toll-like receptor ligands or malaria infection impairs cross-presentation and antiviral immunity. Nat. Immunol. 2006. 7: 165-172.
17. + T cell immunity in mice with anti-dendritic cell HIV gag fusion antibody vaccine. J. Exp. Med. 2006. 203: 607-617.
18. + T cells in a spectrum of human MHC I haplotypes. Proc. Natl. Acad. Sci. USA 2007. 104: 1289-1294.
19. Allan, R. S., Waithman, J., Bedoui, S., Jones, C. M., Villadangos, J. A., Zhan, Y., Lew, A. M. et al., Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 2006. 25: 153-162.
20. + dendritic cells selectively present MHC class I-restricted noncytolytic viral and intracellular bacterial antigens in vivo. J. Immunol. 2005. 175: 196-200.
21. + dendritic cells are generally involved in priming CTL immunity to viruses. J. Immunol. 2004. 172: 1996-2000.
22. Mahnke, K., Qian, Y., Fondel, S., Brueck, J., Becker, C. and Enk, A. H., Targeting of antigens to activated dendritic cells in vivo cures metastatic melanoma in mice. Cancer Res. 2005. 65: 7007-7012.
23. Johnson, T. S., Mahnke, K., Storn, V., Schonfeld, K., Ring, S., Nettelbeck, D. M., Haisma, H. J. et al., Inhibition of melanoma growth by targeting of antigen to dendritic cells via an anti-DEC-205 single-chain fragment variable molecule. Clin. Cancer Res. 2008. 14: 8169-8177.
24. + CTL to cause tumor eradication. J. Immunol. 2004. 173: 6753-6759.
25. + dendritic cells in cross-presentation is not dictated by antigen capture. Proc. Natl. Acad. Sci. USA 2006. 103: 10729-10734.
26. Maraskovsky, E., Brasel, K., Teepe, M., Roux, E. R., Lyman, S. D., Shortman, K. and McKenna, H. J., Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligand-treated mice: multiple dendritic cell subpopulations identified. J. Exp. Med. 1996. 184: 1953-1962.
27. O'Keeffe,M., Hochrein, H., Vremec, D., Pooley, J., Evans, R.,Woulfe, S. and Shortman, K., Effects of administration of progenipoietin 1, Flt-3 ligand, granulocyte colony-stimulating factor, and pegylated granulocyte-macrophage colony-stimulating factor on dendritic cell subsets in mice. Blood 2002. 99: 2122-2130.
28. Brasel, K., De Smedt, T., Smith, J. L. and Maliszewski, C. R., Generation of murine dendritic cells from flt3-ligand-supplemented bone marrow cultures. Blood 2000. 96: 3029-3039.
29. Burgdorf, S., Scholz, C., Kautz, A., Tampe, R. and Kurts, C., Spatial and mechanistic separation of cross-presentation and endogenous antigen presentation. Nat. Immunol. 2008. 9: 558-566.
30. Diener, K. R., Moldenhauer, L. M., Lyons, A. B., Brown, M. P. and Hayball, J. D., Human Flt-3 ligand-mobilized dendritic cells require additional activation to drive effective immune responses. Exp. Hematol. 2008. 36: 51-60.
31. Garulli, B., Stillitano, M. G., Barnaba, V. and Castrucci, M. R., Primary CD8+T-cell response to soluble ovalbumin is improved by chloroquine treatment in vivo. Clin. Vaccine Immunol. 2008. 15: 1497-1504.
32. Klotz, L., Hucke, S., Thimm, D., Classen, S., Gaarz, A., Schultze, J. and Edenhofer, F., Increased antigen cross-presentation but impaired cross-priming after activation of peroxisome proliferator-activated receptor {gamma} is mediated by up-regulation of B7H1. J. Immunol. 2009. 183: 129-136.
33. Li, M., Davey, G. M., Sutherland, R. M., Kurts, C., Lew, A. M., Hirst, C., Carbone, F. R. and Heath, W. R., Cell-associated ovalbumin is cross-presented much more efficiently than soluble ovalbumin in vivo. J. Immunol. 2001. 166: 6099-6103.
34. Merad, M., Sugie, T., Engleman, E. G. and Fong, L., In vivo manipulation of dendritic cells to induce therapeutic immunity. Blood 2002. 99: 1676-1682.
35. O'Keeffe,M., Hochrein, H., Vremec, D., Pooley, J., Evans, R.,Woulfe, S. and Shortman, K., Effects of administration of progenipoietin 1, Flt-3 ligand, granulocyte colony-stimulating factor, and pegylated granulocyte-macrophage colony-stimulating factor on dendritic cell subsets in mice. Blood 2002. 99: 2122-2130.
36. Pulendran, B., Lingappa, J., Kennedy, M. K., Smith, J., Teepe, M., Rudensky, A., Maliszewski, C. R. and Maraskovsky, E., Developmental pathways of dendritic cells in vivo: distinct function, phenotype, and localization of dendritic cell subsets in FLT3 ligand- treated mice. J. Immunol. 1997. 159: 2222-2231.
37. Bedoui, S., Prato, S., Mintern, J., Gebhardt, T., Zhan, Y., Lew, A. M., Heath, W. R. et al., Characterization of an immediate splenic precursor of CD8+ dendritic cells capable of inducing antiviral T cell responses. J. Immunol. 2009. 182: 4200-4207.
38. Longhi, M. P., Trumpfheller, C., Idoyaga, J., Caskey, M., Matos, I., Kluger, C., Salazar, A. M. et al., Dendritic cells require a systemic type I interferon response to induce CD4+ Th1 immunity with poly IC as adjuvant. J. Exp. Med. 2009. 206: 1589-1602.
39. Macagno, A., Napolitani, G., Lanzavecchia, A. and Sallusto, F., Duration, combination and timing: the signal integration model of dendritic cell activation. Trends Immunol. 2007. 28: 227-233.
40. Gil-Torregrosa, B. C., Lennon-Dumenil, A. M., Kessler, B., Guermonprez, P., Ploegh, H. L., Fruci, D., van Endert, P. and Amigorena, S., Control of cross-presentation during dendritic cell maturation. Eur. J. Immunol. 2004. 34: 398-407.
41. Faure, F., Mantegazza, A., Sadaka, C., Sedlik, C., Jotereau, F. and Amigorena, S., Long-lasting cross-presentation of tumor antigen in human DC. Eur. J. Immunol. 2009. 39: 380-390.
42. Delamarre, L., Holcombe, H. and Mellman, I., Presentation of exogenous antigens on major histocompatibility complex (MHC) class I and MHC class II molecules is differentialy regulated during dendritic cell maturation. J. Exp. Med. 2003. 198: 111-122.
43. Wilson, N. S., El-Sukkari, D. and Villadangos, J. A., Dendritic cells constitutively present self antigens in their immature state in vivo and regulate antigen presentation by controlling the rates of MHC class II synthesis and endocytosis. Blood 2004. 103: 2187-2195.
44. Inaba, K., Witmer-Pack, M., Inaba, M., Hathcock, K. S., Sakuta, H., Azuma, M., Yagita, H. et al., The tissue distribution of the B7-2 costimulator in mice: abundant expression on dendritic cells in situ and during maturation in vitro. J. Exp. Med. 1994. 180: 1849-1860.
45. Inaba, K., Turley, S., Iyoda, T., Yamaide, F., Shimoyama, S., Reis e Sousa, C., Germain, R. N. et al., The formation of immunogenic MHC class II- peptide ligands in lysosomal compartments of dendritic cells is regulated by inflammatory stimuli. J. Exp. Med. 2000. 191: 927-936.
46. Inaba, K., Inaba, M., Romani, N., Aya, H., Deguchi, M., Ikehara, S., Muramatsu, S. and Steinman, R. M., Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 1992. 176: 1693-1702.
47. Dudziak, D., Kamphorst, A. O., Heidkamp, G. F., Buchholz, V., Trumpfheller, C., Yamazaki, S., Cheong, C. et al., Differential antigen processing by dendritic cell subsets in vivo. Science 2007. 315: 107-111.
48. Curti, A., Fogli, M., Ratta, M., Tura, S. and Lemoli, R. M., Stem cell factor and FLT3-Ligand are strictly required to sustain the long-term expansion of primitive CD34(1)DR(-) dendritic cell precursors. J. Immunol. 2001. 166: 848-854.
49. D'Amico, A. and Wu, L., The early progenitors of mouse dendritic cells and plasmacytoid predendritic cells are within the bone marrow hemopoietic precursors expressing Flt3. J. Exp. Med. 2003. 198: 293-303.
50. + dendritic cells in vivo. J. Exp. Med. 2003. 198: 305-313.
51. Liu, K., Victora, G. D., Schwickert, T. A., Guermonprez, P., Meredith,M.M., Yao, K., Randolph, G. J. et al., In vivo analysis of dendritic cell development and homeostasis. Science 2009. 324: 392-397.
52. Onai, N., Obata-Onai, A., Tussiwand, R., Lanzavecchia, A. and Manz, M. G., Activation of the Flt3 signal transduction cascade rescues and enhances type I interferon-producing and dendritic cell development. J. Exp. Med. 2006. 203: 227-238.
53. Waskow, C., Liu, K., Darrasse-Jeze, G., Guermonprez, P., Ginhoux, F., Merad, M., Shengelia, T. et al., The receptor tyrosine kinase Flt3 is required for dendritic cell development in peripheral lymphoid tissues. Nat. Immunol. 2008. 9: 676-683.
54. Granelli-Piperno, A., Pritsker, A., Pack, M., Shimeliovich, I., Arrighi, J.-F., Park, C. G., Trumpfheller, C. et al., Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin/CD209 is abundant on macrophages in the normal human lymph node and is not required for dendritic cell stimulation of the mixed leukocyte reaction. J. Immunol. 2005. 175: 4265-4273.
55. Beutler, B., Hoebe, K., Du, X. and Ulevitch, R. J., How we detect microbes and respond to them: the Toll-like receptors and their transducers. J. Leukoc. Biol. 2003. 74: 479-485.
56. Maurer, T., Heit, A., Hochrein, H., Ampenberger, F., O'Keeffe, M., Bauer, S., Lipford, G. et al., CpG-DNA aided cross-presentation of soluble antigens by dendritic cells. Eur. J. Immunol. 2002. 32: 2356-2364.
57. Kurts, C., Miller, J. F., Subramaniam, R. M., Carbone, F. R. and Heath,W. R., Major histocompatibility complex class I-restricted cross-presentation is biased towards high dose antigens and those released during cellular destruction. J. Exp. Med. 1998. 188: 409-414.
58. Jefford, M., Schnurr, M., Toy, T., Masterman, K. A., Shin, A., Beecroft, T., Tai, T. Y. et al., Functional comparison of DCs generated in vivo with Flt3 ligand or in vitro from blood monocytes: differential regulation of function by specific classes of physiologic stimuli. Blood 2003. 102: 1753-1763.
59. Pulendran, B., Banchereau, J., Burkeholder, S., Kraus, E., Guinet, E., Chalouni, C., Caron, D. et al., Flt3-ligand and granulocyte colony-stimulating factor mobilize distinct human dendritic cell subsets in vivo. J. Immunol. 2000. 165: 566-572.
60. Dranoff, G., Jaffee, E., Lazenby, A., Golumbek, P., Levitsky, H., Brose, K., Jackson, V. et al., Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc. Natl. Acad. Sci. USA 1993. 90: 3539-3543.