Accelerated antigen presentation and elicitation of humoral response in vivo by FcγRIIB- and FcγRI/III-mediated immune complex uptake

Cellular Immunology

Volumn 225, Issue 1, 2003, Pages 21-32

  Yada, Ayumi ^a   Ebihara, Shin ^a   Matsumura, Kimio ^a   Endo, Shota ^a   Maeda, Tsutomu ^a   Nakamura, Akira ^a   Akiyama, Kenichi ^a   Aiba, Setsuya ^b   Takai, Toshiyuki ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Antigen presentation; Dendritic cell; Fc receptor; Humoral response; Vaccination

Indexed keywords

FC RECEPTOR; IMMUNOGLOBULIN G; RECEPTOR SUBUNIT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN ANTIBODY COMPLEX; ANTIGEN PRESENTATION; ARTICLE; BONE MARROW; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FEMALE; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IN VIVO STUDY; LANGERHANS CELL; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; MACROPHAGE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; T LYMPHOCYTE; UPREGULATION; WILD TYPE;

EID: 0345414168     PISSN: 00088749     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cellimm.2003.09.008     Document Type: Article

References (44)

1. Banchereau J., Steinman R.M. Dendritic cells and the control of immunity. Nature. 392:1998;245-252.
2. Steinman R.M., Turley S., Mellman I., Inaba K. The induction of tolerance by dendritic cells that have captured apoptotic cells. J. Exp. Med. 191:2000;411-416.
3. Albert M.L., Pearce S.F., Francisco L.M., Sauter B., Roy P., Silverstein R.L., Bhardwaj N. Immature dendritic cells phagocytose apoptotic cells via αvβ5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J. Exp. Med. 188:1998;1359-1368.
4. Binder R.J., Han D.K., Srivastava P.K. CD91: a receptor for heat shock protein gp96. Nat. Immunol. 1:2000;151-155.
5. + cells. J. Immunol. 165:2000;2582-2587.
6. Kato M., Neil T.K., Fearnley D.B., McLellan A.D., Vuckovic S., Hart D.N. Expression of multilectin receptors and comparative FITC-dextran uptake by human dendritic cells. Int. Immunol. 12:2000;1511-1519.
7. Regnault A., Lankar D., Lacabanne V., Rodriguez A., Théry C., Rescigno M., Saito T., Verbeek S., Bonnerot C., Ricciardi-Castagnoli P., Amigorena S. Fcγ receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization. J. Exp. Med. 189:1999;371-380.
8. Maurer D., Fiebiger E., Reininger B., Ebner C., Petzelbauer P., Shi G.-P., Chapman H.A., Stingl G. Fcγ receptor I on dendritic cells delivers IgE-bound multivalent antigens into a cathepsin S-dependent pathway of MHC class II presentation. J. Immunol. 161:1998;2731-2739.
9. Fridman W.H., Bonnerot C., Daëron M., Amigorena S., Teillaud J.L., Sautes C. Structural bases of Fcγ receptor functions. Immunol. Rev. 125:1992;49-76.
10. Daëron M., Latour S., Malbec O., Espinosa E., Pina P., Pasmans S., Fridman W.H. The same tyrosine-based inhibition motif, in the intracytoplasmic domain of FcγRIIB, regulates negatively BCR-, TCR-, and FcR-dependent cell activation. Immunity. 3:1995;635-646.
11. Esposito-Farese M.-E., Sautes C., de La Salle H., Latour S., Bieber T., de La Salle C., Ohlmann P., Fridman W.H., Cazenave J.-P., Teillaud J.-L., Daëron M., Bonnerot C., Hanau D. Membrane and soluble FcγRII/III modulate the antigen-presenting capacity of murine dendritic epidermal Langerhans cells for IgG-complexed antigens. J. Immunol. 155:1995;1725-1736.
12. Minskoff S.A., Matter K., Mellman I. Fc. γ RII-B1 regulates the presentation of B cell receptor-bound antigens J. Immunol. 161:1998;2079-2083.
13. Miettinen H.M., Rose J.K., Mellman I. Fc receptor isoforms exhibit distinct abilities for coated pit localization as a result of cytoplasmic domain heterogeneity. Cell. 58:1989;317-327.
14. Miettinen H.M., Matter K., Hunziker W., Rose J.K., Mellman I. Fc receptor endocytosis is controlled by a cytoplasmic domain determinant that actively prevents coated pit localization. J. Cell Biol. 116:1992;875-888.
15. Amigorena S., Bonnerot C., Drake J.R., Choquet D., Hunziker W., Guillet J.G., Webster P., Sautes C., Mellman I., Fridman W.H. Cytoplasmic domain heterogeneity and functions of IgG Fc receptors in B lymphocytes. Science. 256:1992;1808-1812.
16. Muta T., Kurosaki T., Misulovin Z., Sanchez M., Nussenzweig M.C., Ravetch J.V. A 13-amino-acid motif in the cytoplasmic domain of FcγRIIB modulates B-cell receptor signalling. Nature. 368:1994;70-73.
17. Daëron M. Fc receptor biology. Annu. Rev. Immunol. 15:1997;203-234.
18. Takai T., Ono M., Hikida M., Ohmori H., Ravetch J.V. Augmented humoral and anaphylactic responses in FcγRII-deficient mice. Nature. 379:1996;346-349.
19. Ono M., Bolland S., Tempst P., Ravetch J.V. Role of the inositol phosphatase SHIP in negative regulation of the immune system by the receptor FcγRIIB. Nature. 383:1996;263-266.
20. Takai T. Roles of Fc receptors in autoimmunity. Nat. Rev. Immunol. 2:2002;580-592.
21. Deo Y.M., Graziano R.F., Repp R., van de Winkel J.G.J. Clinical significance of IgG Fc receptors and FcγR-directed immunotherapies. Immunol. Today. 18:1997;127-135.
22. Rudge E.R., Cutler A.J., Pritchard N.R., Smith K.G.C. Interleukin-4 reduces expression of inhibitory receptors on B cells and abolishes CD22 and FcγRII-mediated B cell suppression. J. Exp. Med. 195:2002;1079-1085.
23. Takai T., Li M., Sylvestre D., Clynes R., Ravetch J.V. FcR γ chain deletion results in pleiotrophic effector cell defects. Cell. 76:1994;519-529.
24. Clynes R., Maizes J.S., Guinamard R., Ono M., Takai T., Ravetch J.V. Modulation of immune complex induced inflammation in vivo by the coordinate expression of activation and inhibitory Fc receptors. J. Exp. Med. 189:1999;179-186.
25. Akiyama K., Ebihara S., Yada A., Matsumura K., Aiba S., Nukiwa T., Takai T. Targeting apoptotic tumor cells to Fcγ receptors provides efficient and versatile vaccination against tumors by dendritic cells. J. Immunol. 170:2003;1641-1648.
26. Kalergis A.M., Ravetch J.V. Inducing tumor immunity through the selective engagement of activating Fcγ receptors on dendritic cells. J. Exp. Med. 195:2002;1653-1659.
27. Ujike A., Ishikawa Y., Ono M., Yuasa T., Yoshino T., Fukumoto M., Ravetch J.V., Takai T. Modulation of IgE-mediated systemic anaphylaxis by low affinity Fc receptors for IgG. J. Exp. Med. 189:1999;1573-1579.
28. Unkeless J.C. Characterization of a monoclonal antibody directed against mouse macrophage and lymphocyte Fc receptors. J. Exp. Med. 150:1979;580-596.
29. Ohmori H., Hase N., Hikida M., Takai T., Endo N. Enhancement of antigen-induced interleukin4 and IgE production by specific IgG1 in murine lymphocytes. Cell. Immunol. 145:1992;299-310.
30. Kleine-Tebbe J., Hamilton R.G., Roebber M., Lichtenstein L.M., MacDonald S.M. Purification of immunoglobulin E (IgE) antibodies from sera with high IgE titers. J. Immunol. Methods. 179:1995;153-164.
31. Peng Z., Becker A.B., Simons F.E.R. Binding properties of protein A and protein G for human IgE. Int. Arch. Allergy Immunol. 104:1994;204-206.
32. Inaba K., Inaba M., Romani N., Aya H., Deguchi M., Ikehara S., Muramatsu S., 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. 176:1992;1693-1702.
33. Lutz M.B., Kukutsch N., Ogilvie A.L.J., Robner S., Koch F., Romani N., Chuler G. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods. 223:1999;77-92.
34. Aiba S., Katz S.I. The ability of cultured langerhans cell to process and present protein antigens is MHC-dependent. J. Immunol. 146:1991;2479-2487.
35. Fanger N.A., Voigtlaender D., Liu C., Swink S., Wardwell K., Fisher J., Graziano R.F., Pfefferkorn L.C., Guyre P.M. Characterization of expression, cytokine regulation, and effector function of the high affinity IgG receptor FcγRI (CD64) expressed on human blood dendritic cells. J. Immunol. 158:1997;3090-3098.
36. Sallusto F., Lanzavecchia A. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor. α J. Exp. Med. 179:1994;1109-1118.
37. Barnes N., Gavin A.L., Tan P.S., Mottram P., Koentgen F., Hogarth P.M. FcγRI-deficient mice show multiple alterations to inflammatory and immune responses. Immunity. 16:2002;379-389.
38. Ioan-Facsinay A., de Kimpe S.J., Hellwig S.M., van Lent P.L., Hofhuis F.M., van Ojik H.H., Sedlik C., da Silveira S.A., Gerber J., de Jong Y.F., Roozendaal R., Aarden L.A., van den Berg W.B., Saito T., Mosser D., Amigorena S., Izui S., van Ommen G.J., van Vugt M., van de Winkel J.G., Verbeek J.S. FcγRI (CD64) contributes substantially to severity of arthritis, hypersensitivity responses, and protection from bacterial infection. Immunity. 16:2002;391-402.
39. Amigorena S., Salamero J., Davoust J., Fridman W.H., Bonnerot C. Tyrosine-containing motif that transduces cell activation signals also determines internalization and antigen presentation via type III receptors for IgG. Nature. 358:1992;337-341.
40. Amigorena S., Lankar D., Briken V., Gapin L., Viguier M., Bonnerot C. Type II and III receptors for immunoglobulin G (IgG) control the presentation of different T cell epitopes from single IgG-complexed antigens. J. Exp. Med. 187:1998;505-515.
41. Han S., Zheng B., Schatz D.G., Spanopoulou E., Kelsoe G. Neoteny in lymphocytes: Rag 1 and Rag 2 expression in germinal center B cells. Science. 274:1996;2094-2097.
42. Rafiq K., Bergtold A., Clynes R. Immune complex-mediated antigen presentation induces tumor immunity. J. Clin. Invest. 110:2002;71-79.
43. Wernersson S., Karlsson M.C.I., Dahlstrom J., Mattsson R., Verbeek J.S., Heyman B. IgG-mediated enhancement of antibody responses is low in Fc receptor γ chain-deficient mice and increased in FcγRII-deficient mice. J. Immunol. 163:1999;618-622.
44. Hamano Y., Arase H., Saisho H., Saito T. Immune complex and Fc receptor-mediated augmentation of antigen presentation for in vivo Th cell responses. J. Immunol. 164:2000;6113-6119.