Home LiteratureArticle Details
PMID: 9892619 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Fcgamma receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization.

The Journal of experimental medicine ·Vol. 189 ·No. 2 ·1999-01-18 ·Pages 371-80

Regnault A, Lankar D, Lacabanne V, Rodriguez A, Théry C, Rescigno M, Saito T, Verbeek S, Bonnerot C, Ricciardi-Castagnoli P, Amigorena S

Abstract

Dendritic cells (DCs) express several receptors for the Fc portion of immunoglobulin (Ig)G (FcgammaR), which mediate internalization of antigen-IgG complexes (immune complexes, ICs) and promote efficient major histocompatibility complex (MHC) class II-restricted antigen presentation. We now show that FcgammaRs have two additional specific attributes in murine DCs: the induction of DC maturation and the promotion of efficient MHC class I-restricted presentation of peptides from exogenous, IgG-complexed antigens. Both FcgammaR functions require the FcgammaR-associated gamma chain. FcgammaR-mediated MHC class I-restricted antigen presentation is extremely sensitive and specific to immature DCs. It requires proteasomal degradation and is dependent on functional peptide transporter associated with antigen processing, TAP1-TAP2. By promoting DC maturation and presentation on both MHC class I and II molecules, ICs should efficiently sensitize DCs for priming of both CD4(+) helper and CD8(+) cytotoxic T lymphocytes in vivo.

MeSH Terms
ATP Binding Cassette Transporter, Subfamily B, Member 2 ATP Binding Cassette Transporter, Subfamily B, Member 3 ATP-Binding Cassette Transporters/immunology Animals Antigen Presentation/immunology Antigen-Antibody Complex/immunology Antigens, CD/immunology Bone Marrow/immunology Cysteine Endopeptidases/metabolism Dendritic Cells/immunology Fluorescent Antibody Technique Histocompatibility Antigens Class I/immunology Immunoglobulin G/immunology Lipopolysaccharides/pharmacology Mice Mice, Knockout Multienzyme Complexes/metabolism Ovalbumin/immunology Proteasome Endopeptidase Complex Receptors, IgG/immunology
Chemicals
ATP Binding Cassette Transporter, Subfamily B, Member 2 ATP Binding Cassette Transporter, Subfamily B, Member 3 ATP-Binding Cassette Transporters Antigen-Antibody Complex Antigens, CD Histocompatibility Antigens Class I Immunoglobulin G Lipopolysaccharides Multienzyme Complexes Receptors, IgG TAP1 protein, human Tap1 protein, mouse Tap2 protein, mouse TAP2 protein, human Ovalbumin Cysteine Endopeptidases Proteasome Endopeptidase Complex
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Regnault A
Institut National de la Santé et de la Recherche Médicale CJF 95-01, Institut Curie, Section Recherche, 75005 Paris, France.
Lankar D
Lacabanne V
Rodriguez A
Théry C
Rescigno M
Saito T
Verbeek S
Bonnerot C
Ricciardi-Castagnoli P
Amigorena S
References (43)
43 references, click to expand
  1. TAP1 mutant mice are deficient in antigen presentation, surface class I molecules, and CD4-8+ T cells.
    Cell. 1992 Dec 24;71(7):1205-14 PMID: 1473153
  2. The endocytic activity of dendritic cells.
    J Exp Med. 1995 Aug 1;182(2):283-8 PMID: 7629494
  3. Role of associated gamma-chain in tyrosine kinase activation via murine Fc gamma RIII.
    EMBO J. 1992 Jul;11(7):2747-57 PMID: 1321036
  4. A conditioned dendritic cell can be a temporal bridge between a CD4+ T-helper and a T-killer cell.
    Nature. 1998 Jun 4;393(6684):474-8 PMID: 9624003
  5. LacZ inducible, antigen/MHC-specific T cell hybrids.
    Int Immunol. 1994 Mar;6(3):369-76 PMID: 8186188
  6. FcR gamma-chain is essential for both surface expression and function of human Fc gamma RI (CD64) in vivo.
    Blood. 1996 May 1;87(9):3593-9 PMID: 8611682
  7. Class I MHC presentation of exogenous soluble antigen via macropinocytosis in bone marrow macrophages.
    Immunity. 1995 Dec;3(6):783-91 PMID: 8777723
  8. Capture and processing of exogenous antigens for presentation on MHC molecules.
    Annu Rev Immunol. 1997;15:821-50 PMID: 9143708
  9. Fc receptors.
    Annu Rev Immunol. 1991;9:457-92 PMID: 1910686
  10. Role of B-cell and Fc receptors in the selection of T-cell epitopes.
    Curr Opin Immunol. 1998 Feb;10(1):88-92 PMID: 9523117
  11. Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin.
    Science. 1995 May 5;268(5211):726-31 PMID: 7732382
  12. Dendritic cell/macrophage precursors capture exogenous antigen for MHC class I presentation by dendritic cells.
    Eur J Immunol. 1998 Jun;28(6):1923-33 PMID: 9645374
  13. Constitutive macropinocytosis allows TAP-dependent major histocompatibility complex class I presentation of exogenous soluble antigen by bone marrow-derived dendritic cells.
    Eur J Immunol. 1997 Jan;27(1):280-8 PMID: 9022030
  14. Presentation of exogenous antigen with class I major histocompatibility complex molecules.
    Science. 1990 Aug 24;249(4971):918-21 PMID: 2392683
  15. Bacteria-induced neo-biosynthesis, stabilization, and surface expression of functional class I molecules in mouse dendritic cells.
    Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):5229-34 PMID: 9560258
  16. Nucleotide sequences of three H-2K and three H-2D complementary DNA clones coding mouse class I MHC heavy chain proteins.
    Ann Transplant. 1996;1(3):26-31 PMID: 9869916
  17. Antigen specificity and cross-reactivity of monoclonal anti-lysozyme antibodies.
    Mol Immunol. 1987 Feb;24(2):97-108 PMID: 2441250
  18. Help for cytotoxic-T-cell responses is mediated by CD40 signalling.
    Nature. 1998 Jun 4;393(6684):478-80 PMID: 9624004
  19. Dendritic cells and the control of immunity.
    Nature. 1998 Mar 19;392(6673):245-52 PMID: 9521319
  20. Major histocompatibility complex class I presentation of peptides derived from soluble exogenous antigen by a subset of cells engaged in phagocytosis.
    J Exp Med. 1995 Sep 1;182(3):841-51 PMID: 7650490
  21. Antigen recognition by class I-restricted T lymphocytes.
    Annu Rev Immunol. 1989;7:601-24 PMID: 2469442
  22. CD4-deficient mice have reduced levels of memory cytotoxic T lymphocytes after immunization and show diminished resistance to subsequent virus challenge.
    J Virol. 1996 Feb;70(2):1072-9 PMID: 8551565
  23. Tyrosine-containing motif that transduces cell activation signals also determines internalization and antigen presentation via type III receptors for IgG.
    Nature. 1992 Jul 23;358(6384):337-41 PMID: 1386408
  24. Cross-priming for a secondary cytotoxic response to minor H antigens with H-2 congenic cells which do not cross-react in the cytotoxic assay.
    J Exp Med. 1976 May 1;143(5):1283-8 PMID: 1083422
  25. Phagocytic processing of bacterial antigens for class I MHC presentation to T cells.
    Nature. 1993 Jan 28;361(6410):359-62 PMID: 7678924
  26. Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs.
    Nature. 1998 Mar 5;392(6671):86-9 PMID: 9510252
  27. Fc receptors: rubor redux.
    Cell. 1994 Aug 26;78(4):553-60 PMID: 8069908
  28. 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 alpha.
    J Exp Med. 1994 Apr 1;179(4):1109-18 PMID: 8145033
  29. Progressive loss of CD8+ T cell-mediated control of a gamma-herpesvirus in the absence of CD4+ T cells.
    J Exp Med. 1996 Sep 1;184(3):863-71 PMID: 9064346
  30. Mechanisms of antigen uptake for presentation.
    Curr Opin Immunol. 1996 Jun;8(3):348-54 PMID: 8794000
  31. Characterization of expression, cytokine regulation, and effector function of the high affinity IgG receptor Fc gamma RI (CD64) expressed on human blood dendritic cells.
    J Immunol. 1997 Apr 1;158(7):3090-8 PMID: 9120261
  32. Induction of a CD8+ cytotoxic T lymphocyte response by cross-priming requires cognate CD4+ T cell help.
    J Exp Med. 1997 Jul 7;186(1):65-70 PMID: 9206998
  33. Cytoplasmic domain heterogeneity and functions of IgG Fc receptors in B lymphocytes.
    Science. 1992 Jun 26;256(5065):1808-12 PMID: 1535455
  34. Helper activity is required for the in vivo generation of cytotoxic T lymphocytes.
    J Exp Med. 1982 Mar 1;155(3):768-82 PMID: 6801178
  35. A phagosome-to-cytosol pathway for exogenous antigens presented on MHC class I molecules.
    Science. 1995 Jan 13;267(5195):243-6 PMID: 7809629
  36. Role of bone marrow-derived cells in presenting MHC class I-restricted tumor antigens.
    Science. 1994 May 13;264(5161):961-5 PMID: 7513904
  37. Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells.
    Nature. 1997 Aug 21;388(6644):782-7 PMID: 9285591
  38. Identification, molecular cloning, biologic properties, and tissue distribution of a novel isoform of murine low-affinity IgG receptor homologous to human Fc gamma RIIB1.
    J Immunol. 1996 Jul 1;157(1):189-97 PMID: 8683114
  39. Dendritic cells but not B cells present antigenic complexes to class II-restricted T cells after administration of protein in adjuvant.
    J Exp Med. 1996 Mar 1;183(3):751-7 PMID: 8642279
  40. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions.
    Nature. 1998 Jun 4;393(6684):480-3 PMID: 9624005
  41. Developmental regulation of MHC class II transport in mouse dendritic cells.
    Nature. 1997 Aug 21;388(6644):787-92 PMID: 9285592
  42. Maturation stages of mouse dendritic cells in growth factor-dependent long-term cultures.
    J Exp Med. 1997 Jan 20;185(2):317-28 PMID: 9016880
  43. Dendritic cells: unique leukocyte populations which control the primary immune response.
    Blood. 1997 Nov 1;90(9):3245-87 PMID: 9345009
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
1999-01-18
Pages
371-80
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2192989
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]