The linkage of innate to adaptive immunity via maturing dendritic cells in vivo requires CD40 ligation in addition to antigen presentation and CD80/86 costimulation

Journal of Experimental Medicine

Volumn 199, Issue 12, 2004, Pages 1607-1618

  Fujii, Shin Ichiro ^a   Liu, Kang ^a   Smith, Caroline ^a   Bonito, Anthony J ^a   Steinman, Ralph M ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

galactosylceramide; CD40; Maturation; NKT; TNF

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; B7 ANTIGEN; CD4 ANTIGEN; CD40 ANTIGEN; CD40 LIGAND; CD8 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 12; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; OVALBUMIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ARTICLE; CELL MATURATION; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; FLOW CYTOMETRY; IMMUNITY; IMMUNOSTIMULATION; MIXED LYMPHOCYTE REACTION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; TH1 CELL;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD40; ANTIGENS, CD80; ANTIGENS, CD86; CD40 LIGAND; DENDRITIC CELLS; FEMALE; IMMUNITY, CELLULAR; INTERFERON TYPE II; LYMPHOCYTE ACTIVATION; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SPLEEN; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 3042545974     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20040317     Document Type: Article

References (57)

1. Heath, W.R., and F.R. Carbone. 2001. Cross-presentation, dendritic cells, tolerance and immunity. Annu. Rev. Immunol. 19:47-64.
2. Moser, M. 2003. Dendritic cells in immunity and tolerance-do they display opposite functions? Immunity. 19:5-8.
3. Steinman, R.M., and M.C. Nussenzweig. 2002. Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance. Proc. Natl. Acad. Sci. USA. 99:351-358.
4. De Smedt, T., B. Pajak, E. Muraille, L. Lespagnard, E. Heinen, P. De Baetselier, J. Urbain, O. Leo, and M. Moser. 1996. Regulation of dendritic cell numbers and maturation by lipopolysaccharide in vivo. J. Exp. Med. 184:1413-1424.
5. Sparwasser, T., R.M. Vabulas, B. Villmow, G.B. Lipford, and H. Wagner. 2000. Bacterial CpG-DNA activates dendritic cells in vivo: T helper cell-independent cytotoxic T cell responses to soluble proteins. Eur. J. Immunol. 30:3591-3597.
6. Kamath, A.T., J. Pooley, M.A. O'Keeffe, D. Vremec, Y. Zhan, A. Lew, A. D'Amico, L. Wu, D.F. Tough, and K.S. Shortman. 2000. The development, maturation, and turnover rate of mouse spleen dendritic cell populations. J. Immunol. 165:6762-6770.
7. + dendritic cell subset selectively endocytoses dying cells in culture and in vivo. J. Exp. Med. 195:1289-1302.
8. Liu, K., T. Iyoda, M. Saternus, K. Kimura, K. Inaba, and R.M. Steinman. 2002. Immune tolerance after delivery of dying cells to dendritic cells in situ. J. Exp. Med. 196:1091-1097.
9. Hawiger, D., K. Inaba, Y. Dorsett, K. 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. 194:769-780.
10. + T cell tolerance. J. Exp. Med. 196:1627-1638.
11. Wilson, N.S., El-Sukkari, G.T. Belz, C.M. Smith, R.J. Steptoe, W.R. Heath, K. Shortman, and J.A. Villadangos. 2003. Most lymphoid organ dendritic cell types are phenotypically and functionally immature. Blood. 102:2187-2194.
12. Hawiger, D., R.F. Masilamani, E. Bettelli, V.K. Kuchroo, and M.C. Nussenzweig. 2004. Dynamic regulation of T cell tolerance induced by dendritic cells in vivo. Immunity. In press.
13. + regulatory T cells by antigen processing dendritic cells. J. Exp. Med. 198:235-247.
14. Brimnes, M.K., L. Bonifaz, R.M. Steinman, and T.M. Moran. 2003. Influenza virus-induced dendritic cell maturation is associated with the induction of strong T cell immunity to a coadministered, normally nonimmunogenic protein. J. Exp. Med. 198:133-144.
15. Fujii, S., K. Shimizu, C. Smith, L. Bonifaz, and R.M. Steinman. 2003. Activation of natural killer T cells by α-galactosylceramide rapidly induces the full maturation of dendritic cells in vivo and thereby acts as an adjuvant for combined CD4 and CD8 T cell immunity to a coadministered protein. J. Exp. Med. 198:267-279.
16. + T cell responses to soluble antigen in vivo through direct interaction with dendritic cells. J. Immunol. 171:5140-5147.
17. 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 the DEC-205 receptor on maturing dendritic cells improves T cell vaccination. J. Exp. Med. 199:815-824.
18. Kawano, T., J. Cui, Y. Koezuka, I. Toura, Y. Kaneko, K. Motoki, H. Ueno, R. Nakagawa, H. Sato, E. Kondo, et al. 1997. CD1d-restricted and TCR-mediated activation of Va14 NKT cells by glycosylceramides. Science. 278:1626-1629.
19. Gonzalez-Aseguinolaza, G., L. Van Kaer, C.C. Bergmann, J.M. Wilson, J. Schmieg, M. Kronenberg, T. Nakayama, M. Taniguchi, Y. Koezuka, and M. Tsuji. 2002. Natural killer T cell ligand α-galactosylceramide enhances protective immunity induced by malaria vaccines. J. Exp. Med. 195:617-624.
20. Shah, J.A., P.A. Darrah, D.R. Ambrozak, T.N. Turon, S. Mendez, J. Kirman, C.Y. Wu, N. Glaichenhaus, and R.A. Seder. 2003. Dendritic cells are responsible for the capacity of CpG oligodeoxynucleotides to act as an adjuvant for protective vaccine immunity against Leishmania major in mice. J. Exp. Med. 198:281-291.
21. Caux, C., C. Massacrier, B. Vanbervliet, B. Dubois, C. Van Kooten, I. Durand, and J. Banchereau. 1994. Activation of human dendritic cells through CD40 cross-linking. J. Exp. Med. 180:1263-1272.
22. + hematopoietic progenitors induces their proliferation and differentiation into functional dendritic cells. J. Exp. Med. 185:341-349.
23. Delamarre, L., H. Holcombe, and I. Mellman. 2003. 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. 198:111-122.
24. Machy, P., K. Serre, M. Baillet, and L. Leserman. 2002. Induction of MHC class I presentation of exogenous antigen by dendritic cells is controlled by CD4(+) T cells engaging class II molecules in cholesterol-rich domains. J. Immunol. 168: 1172-1180.
25. Cella, M., D. Scheidegger, K. Palmer-Lehmann, P. Lane, A. Lanzavecchia, and G. Alber. 1996. Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J. Exp. Med. 184:747-752.
26. Koch, F., U. Stanzl, P. Jennewien, K. Janke, C. Heufler, E. Kämpgen, N. Romani, and G. Schuler. 1996. High level IL-12 production by murine dendritic cells: upregulation via MHC class II and CD40 molecules and downregulation by IL-4 and IL-10. J. Exp. Med. 184:741-746.
27. + T helper and a T-killer cell. Nature. 393:474-478.
28. Bennett, S.R.M., F.R. Carbone, F. Karamalis, R.A. Flavell, J.F.A.P. Miller, and W.R. Heath. 1998. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature. 393: 478-480.
29. Schoenberger, S.P., R.E.M. Toes, E.I.H. van der Voort, R. Offringa, and C.J.M. Melief. 1998. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature. 393:480-483.
30. Inaba, K., N. Romani, G. Schuler, A. Mirza, and K.M. Steinman. 1997. Generation of dendritic cells from proliferating mouse bone marrow progenitors. In Current Protocols in Immunology. J.E. Coligan, A.M. Kruisbeek, D.H. Margulies, E.M. Shevach, and W. Strober, editors. Greene Publishing Associates and Wiley-Interscience, New York. 3.7.7-3.7.15.
31. Sallusto, F., and A. Lanzavecchia. 1994. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and down-regulated by tumor necrosis factor α. J. Exp. Med. 179:1109-1118.
32. Inaba, K., S. Turley, T. Iyoda, F. Yamaide, S. Shimoyama, C. Reis e Sousa, R.N. Germain, I. Mellman, and R.M. Steinman. 2000. The formation of immunogenic MHC class II-peptide ligands in lysosomal compartments of dendritic cells is regulated by inflammatory stimuli. J. Exp. Med. 191:927-936.
33. Le Bon, A., G. Schiavoni, G. D'Agostinio, I. Gresser, F. Belardelli, and D.F. Tough. 2001. Type I interferons potently enhance humoral immunity and can promote isotype switching by stimulating dendritic cells in vivo. Immunity. 14:461-470.
34. Matsuda, J.L., O.V. Naidenko, L. Gapin, T. Nakayama, M. Taniguchi, C.R. Wang, Y. Koezuka, and M. Kronenberg. 2000. Tracking the response of natural killer T cells to a glycolipid antigen using CD1d tetramers. J. Exp. Med. 192:741-754.
35. Hochrein, H., K. Shortman, D. Vremec, B. Scott, P. Hertzog, and M. O'Keeffe. 2001. Differential production of IL-12, IFN-a, and IFN-g by mouse dendritic cell subsets. J. Immunol. 166:5448-5455.
36. Kitamura, H., A. Ohta, M. Sekimoto, M. Sato, K. Iwakabe, M. Nakui, T. Yahata, H. Meng, T. Koda, S. Nishimura, et al. 2000. a-Galactosylceramide induces early B-cell activation through IL-4 production by NKT cells. Cell. Immunol. 199:37-42.
37. Matsuda, J.L., L. Gapin, J.L. Baron, S. Sidobre, D.B. Stetson, M. Mohrs, R.M. Locksley, and M. Kronenberg. 2003. Mouse Va14i natural killer T cells are resistant to cytokine polarization in vivo. Proc. Natl. Acad. Sci. USA. 100:8395-8400.
38. + NKT cells: stimulation of IL-12 production by antigen-presenting cells in the innate immune system. J. Immunol. 163:93-101.
39. Limmer, A., J. Ohl, C. Kurts, H.G. Ljunggren, Y. Reiss, M. Groettrup, F. Momburg, B. Arnold, and P.A. Knolle. 2000. Efficient presentation of exogenous antigen by liver endothelial cells to CD8+ T cells results in antigen-specific T-cell tolerance. Natl. Med. 6:1348-1354.
40. + T cell help. J. Exp. Med. 186:65-70.
41. Schulz, O., A.D. Edwards, M. Schito, J. Aliberti, S. Manickasingham, A. Sher, and C. Reis e Sousa. 2000. CD40 triggering of heterodimeric IL-12 p70 production by dendritic cells in vivo requires a microbial priming signal. Immunity. 13: 453-462.
42. Edwards, A.D., S.P. Manickasingham, R. Sporri, S.S. Diebold, O. Schulz, A. Sher, T. Kaisho, S. Akira, and E.S.C. Reis. 2002. Microbial recognition via toll-like receptor-dependent and -independent pathways determines the cytokine response of murine dendritic cell subsets to CD40 triggering. J. Immunol. 169:3652-3660.
43. Sporri, R., and E.S.C. Reis. 2003. Newly activated T cells promote maturation of bystander dendritic cells but not IL-12 production. J. Immunol. 171:6406-6413.
44. + cytotoxic T lymphocyte priming capacity upon activation by T helper cell-independent or -dependent stimuli. J. Exp. Med. 192:145-150.
45. Schuler, G., and R.M. Steinman. 1985. Murine epidermal Langerhans cells mature into potent immunostimulatory dendritic cells in vitro. J. Exp. Med. 161:526-546.
46. Inaba, K., G. Schuler, M.D. Witmer, J. Valinsky, B. Atassi, and R.M. Steinman. 1986. The immunologic properties of purified Langerhans cells: distinct requirements for the stimulation of unprimed and sensitized T lymphocytes. J. Exp. Med. 164:605-613.
47. Romani, N., S. Koide, M. Crowley, M. Witmer-Pack, A.M. Livingstone, C.G. Fathman, K. Inaba, and R.M. Steinman. 1989. Presentation of exogenous protein antigens by dendritic cells to T cell clones: intact protein is presented best by immature, epidermal Langerhans cells. J. Exp. Med. 169: 1169-1178.
48. Romani, N., K. Inaba, E. Pure, M. Crowley, M. Witmer-Pack, and R.M. Steinman. 1989. A small number of anti-CD3 molecules on dendritic cells stimulate DNA synthesis in mouse T lymphocytes. J. Exp. Med. 169:1153-1168.
49. Albert, M.L., M. Jegathesan, and R.B. Darnell. 2001. Dendritic cell maturation is required for the cross-tolerization of CD8+ T cells. Nat. Immunol. 2:1010-1017.
50. Henn, V., J.R. Slupsky, M. Grafe, I. Anagnostopoulos, R. Forster, G. Muller-Berghaus, and R.A. Kroczek. 1998. CD40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells. Nature. 391:591-594.
51. Millar, D.G., K.M. Garza, B. Odermatt, A.R. Elford, N. Ono, Z. Li, and P.S. Ohashi. 2003. Hsp70 promotes antigen-presenting cell function and converts T-cell tolerance to autoimmunity in vivo. Nat. Med. 9:1469-1476.
52. Josien, R. H.-L. Hi, E. Ingulli, S. Sarma, B.R. Wong, M. Vologodskaia, R.M. Steinman, and Y. Choi. 2000. TRANCE, a tumor necrosis family member, enhances the longevity and adjuvant properties of dendritic cells in vivo. J. Exp. Med. 191:495-501.
53. Moodycliffe, A.M., V. Shreedhar, S.E. Ullrich, J. Walterscheid, C. Bucana, M.L. Kripke, and L. Flores-Romo. 2000. CD40-CD40 ligand interactions in vivo regulate migration of antigen-bearing dendritic cells from the skin to draining lymph nodes. J. Exp. Med. 191:2011-2020.
54. + T cells. Immunity. 19:877-889.
55. Grohmann, U., F. Fallarino, S. Silla, R. Bianchi, M.L. Belladonna, C. Vacca, A. Micheletti, M.C. Fioretti, and P. Puccetti. 2001. CD40 ligation ablates the tolerogenic potential of lymphoid dendritic cells. J. Immunol. 166:277-283.
56. Labeur, M.S., B. Roters, B. Pers, A. Mehling, T.A. Luger, T. Schwarz, and S. Grabbe. 1999. Generation of tumor immunity by bone marrow-derived dendritic cells correlates with dendritic cell maturation stage. J. Immunol. 162:168-175.
57. + T cells in vitro, whereas CD40 ligation is essential. J. Immunol. 167:6247-6255.