Skip to main content
PMC home page
Immunology logoLink to Immunology
. 1998 Jul;94(3):318–324. doi: 10.1046/j.1365-2567.1998.00525.x

Specific antigen targeting to surface IgE and IgG on mouse bone marrow-derived mast cells enhances efficiency of antigen presentation.

C Tkaczyk 1, M Viguier 1, Y Boutin 1, P Frandji 1, B David 1, J Hébert 1, S Mécheri 1
PMCID: PMC1364248  PMID: 9767412

Abstract

The discovery that bone marrow-derived mast cells can express major histocompatibility complex class II molecules and act as antigen-presenting cells prompted us to evaluate this function when antigen is internalized through fluid-phase endocytosis or via specific uptake by using IgG and IgE antibodies. This study was performed using a specific T-cell hybridoma developed against Lol p 1, the major allergen of grass pollen Lolium perenne. Expression of Fc gamma R and Fc epsilon RI by mast cells led us to investigate the influence of IgG- and IgE-targeted antigen on the antigen-presenting function of mast cells. Internalization of Lol p 1 through different specific IgG monoclonal antibodies (mAb) resulted in the activation of Lol p 1-specific T-cell hybridoma at concentrations about 100-fold less than that required for T-cell stimulation by uncomplexed antigen. IgE-complexed Lol p 1, which facilitates trapping of antigen by mast cells, induced an accelerated and more efficient antigen-presenting capacity of mast cells than that obtained with uncomplexed antigen. However, aggregation of anti-dinitrophenyl (DNP) IgE mAb by the irrelevant antigen DNP-human serum albumin did not substantially increase the capacity of mast cells to present Lol p 1 to T cells. This suggests that the mere aggregation of Fc epsilon RI is not sufficient for enhanced antigen presentation mediated by IgE. Tissue distribution and strategic location of mast cells at the mucosal barriers and their capacity to process the antigen through efficient fluid-phase pinocytosis as well as IgG- and IgE-dependent targeting of antigens provide mast cells with a prominent role in immune surveillance.

Full text

PDF
323

Images in this article

321Figure 1
on p.321

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ashwell J. D., DeFranco A. L., Paul W. E., Schwartz R. H. Antigen presentation by resting B cells. Radiosensitivity of the antigen-presentation function and two distinct pathways of T cell activation. J Exp Med. 1984 Mar 1;159(3):881–905. doi: 10.1084/jem.159.3.881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berg M., Uellner R., Langhorne J. Fc gamma receptor II dependency of enhanced presentation of major histocompatibility complex class II peptides by a B cell lymphoma. Eur J Immunol. 1997 Apr;27(4):1022–1028. doi: 10.1002/eji.1830270432. [DOI] [PubMed] [Google Scholar]
  3. Berzofsky J. A. T-B reciprocity. An Ia-restricted epitope-specific circuit regulating T cell-B cell interaction and antibody specificity. Surv Immunol Res. 1983;2(3):223–229. doi: 10.1007/BF02918417. [DOI] [PubMed] [Google Scholar]
  4. Bieber T., de la Salle H., Wollenberg A., Hakimi J., Chizzonite R., Ring J., Hanau D., de la Salle C. Human epidermal Langerhans cells express the high affinity receptor for immunoglobulin E (Fc epsilon RI). J Exp Med. 1992 May 1;175(5):1285–1290. doi: 10.1084/jem.175.5.1285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boutin Y., Lamontagne P., Boulanger J., Brunet C., Hébert J. Immunological and biological properties of recombinant Lol p 1. Int Arch Allergy Immunol. 1997 Mar;112(3):218–225. doi: 10.1159/000237457. [DOI] [PubMed] [Google Scholar]
  6. Burd P. R., Rogers H. W., Gordon J. R., Martin C. A., Jayaraman S., Wilson S. D., Dvorak A. M., Galli S. J., Dorf M. E. Interleukin 3-dependent and -independent mast cells stimulated with IgE and antigen express multiple cytokines. J Exp Med. 1989 Jul 1;170(1):245–257. doi: 10.1084/jem.170.1.245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Casten L. A., Pierce S. K. Receptor-mediated B cell antigen processing. Increased antigenicity of a globular protein covalently coupled to antibodies specific for B cell surface structures. J Immunol. 1988 Jan 15;140(2):404–410. [PubMed] [Google Scholar]
  8. Chesnut R. W., Grey H. M. Studies on the capacity of B cells to serve as antigen-presenting cells. J Immunol. 1981 Mar;126(3):1075–1079. [PubMed] [Google Scholar]
  9. Fox C. C., Jewell S. D., Whitacre C. C. Rat peritoneal mast cells present antigen to a PPD-specific T cell line. Cell Immunol. 1994 Oct 1;158(1):253–264. doi: 10.1006/cimm.1994.1272. [DOI] [PubMed] [Google Scholar]
  10. Frandji P., Mourad W., Tkaczyk C., Singer M., David B., Colle J. H., Mécheri S. IL-4 mRNA transcription is induced in mouse bone marrow-derived mast cells through an MHC class II-dependent signaling pathway. Eur J Immunol. 1998 Mar;28(3):844–854. doi: 10.1002/(SICI)1521-4141(199803)28:03<844::AID-IMMU844>3.0.CO;2-4. [DOI] [PubMed] [Google Scholar]
  11. Frandji P., Oskéritzian C., Cacaraci F., Lapeyre J., Peronet R., David B., Guillet J. G., Mécheri S. Antigen-dependent stimulation by bone marrow-derived mast cells of MHC class II-restricted T cell hybridoma. J Immunol. 1993 Dec 1;151(11):6318–6328. [PubMed] [Google Scholar]
  12. Frandji P., Tkaczyk C., Oskéritzian C., Lapeyre J., Peronet R., David B., Guillet J. G., Mécheri S. Presentation of soluble antigens by mast cells: upregulation by interleukin-4 and granulocyte/macrophage colony-stimulating factor and downregulation by interferon-gamma. Cell Immunol. 1995 Jun;163(1):37–46. doi: 10.1006/cimm.1995.1096. [DOI] [PubMed] [Google Scholar]
  13. Gustavsson S., Hjulström S., Liu T., Heyman B. CD23/IgE-mediated regulation of the specific antibody response in vivo. J Immunol. 1994 May 15;152(10):4793–4800. [PubMed] [Google Scholar]
  14. Heyman B., Tianmin L., Gustavsson S. In vivo enhancement of the specific antibody response via the low-affinity receptor for IgE. Eur J Immunol. 1993 Jul;23(7):1739–1742. doi: 10.1002/eji.1830230754. [DOI] [PubMed] [Google Scholar]
  15. Jelachich M. L., Lakey E. K., Casten L., Pierce S. K. Antigen presentation is a function of all B cell subpopulations separated on the basis of size. Eur J Immunol. 1986 Apr;16(4):411–416. doi: 10.1002/eji.1830160417. [DOI] [PubMed] [Google Scholar]
  16. Kehry M. R., Yamashita L. C. Low-affinity IgE receptor (CD23) function on mouse B cells: role in IgE-dependent antigen focusing. Proc Natl Acad Sci U S A. 1989 Oct;86(19):7556–7560. doi: 10.1073/pnas.86.19.7556. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kraal G., Breel M., Janse M., Bruin G. Langerhans' cells, veiled cells, and interdigitating cells in the mouse recognized by a monoclonal antibody. J Exp Med. 1986 Apr 1;163(4):981–997. doi: 10.1084/jem.163.4.981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Krieger J. I., Grammer S. F., Grey H. M., Chesnut R. W. Antigen presentation by splenic B cells: resting B cells are ineffective, whereas activated B cells are effective accessory cells for T cell responses. J Immunol. 1985 Nov;135(5):2937–2945. [PubMed] [Google Scholar]
  19. Lanzavecchia A. Antigen presentation by B lymphocytes: a critical step in T-B collaboration. Curr Top Microbiol Immunol. 1986;130:65–78. doi: 10.1007/978-3-642-71440-5_6. [DOI] [PubMed] [Google Scholar]
  20. Lanzavecchia A. Antigen-specific interaction between T and B cells. Nature. 1985 Apr 11;314(6011):537–539. doi: 10.1038/314537a0. [DOI] [PubMed] [Google Scholar]
  21. Liu F. T., Bohn J. W., Ferry E. L., Yamamoto H., Molinaro C. A., Sherman L. A., Klinman N. R., Katz D. H. Monoclonal dinitrophenyl-specific murine IgE antibody: preparation, isolation, and characterization. J Immunol. 1980 Jun;124(6):2728–2737. [PubMed] [Google Scholar]
  22. Manca F., Kunkl A., Fenoglio D., Fowler A., Sercarz E., Celada F. Constraints in T-B cooperation related to epitope topology on E. coli beta-galactosidase. I. The fine specificity of T cells dictates the fine specificity of antibodies directed to conformation-dependent determinants. Eur J Immunol. 1985 Apr;15(4):345–350. doi: 10.1002/eji.1830150408. [DOI] [PubMed] [Google Scholar]
  23. Maurer D., Ebner C., Reininger B., Fiebiger E., Kraft D., Kinet J. P., Stingl G. The high affinity IgE receptor (Fc epsilon RI) mediates IgE-dependent allergen presentation. J Immunol. 1995 Jun 15;154(12):6285–6290. [PubMed] [Google Scholar]
  24. Maurer D., Fiebiger E., Reininger B., Wolff-Winiski B., Jouvin M. H., Kilgus O., Kinet J. P., Stingl G. Expression of functional high affinity immunoglobulin E receptors (Fc epsilon RI) on monocytes of atopic individuals. J Exp Med. 1994 Feb 1;179(2):745–750. doi: 10.1084/jem.179.2.745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pirron U., Schlunck T., Prinz J. C., Rieber E. P. IgE-dependent antigen focusing by human B lymphocytes is mediated by the low-affinity receptor for IgE. Eur J Immunol. 1990 Jul;20(7):1547–1551. doi: 10.1002/eji.1830200721. [DOI] [PubMed] [Google Scholar]
  26. Plaut M., Pierce J. H., Watson C. J., Hanley-Hyde J., Nordan R. P., Paul W. E. Mast cell lines produce lymphokines in response to cross-linkage of Fc epsilon RI or to calcium ionophores. Nature. 1989 May 4;339(6219):64–67. doi: 10.1038/339064a0. [DOI] [PubMed] [Google Scholar]
  27. Razin E., Cordon-Cardo C., Good R. A. Growth of a pure population of mouse mast cells in vitro with conditioned medium derived from concanavalin A-stimulated splenocytes. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2559–2561. doi: 10.1073/pnas.78.4.2559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rock K. L., Benacerraf B., Abbas A. K. Antigen presentation by hapten-specific B lymphocytes. I. Role of surface immunoglobulin receptors. J Exp Med. 1984 Oct 1;160(4):1102–1113. doi: 10.1084/jem.160.4.1102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Simitsek P. D., Campbell D. G., Lanzavecchia A., Fairweather N., Watts C. Modulation of antigen processing by bound antibodies can boost or suppress class II major histocompatibility complex presentation of different T cell determinants. J Exp Med. 1995 Jun 1;181(6):1957–1963. doi: 10.1084/jem.181.6.1957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Snider D. P., Segal D. M. Efficiency of antigen presentation after antigen targeting to surface IgD, IgM, MHC, Fc gamma RII, and B220 molecules on murine splenic B cells. J Immunol. 1989 Jul 1;143(1):59–65. [PubMed] [Google Scholar]
  31. Tony H. P., Parker D. C. Major histocompatibility complex-restricted, polyclonal B cell responses resulting from helper T cell recognition of antiimmunoglobulin presented by small B lymphocytes. J Exp Med. 1985 Jan 1;161(1):223–241. doi: 10.1084/jem.161.1.223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wang B., Rieger A., Kilgus O., Ochiai K., Maurer D., Födinger D., Kinet J. P., Stingl G. Epidermal Langerhans cells from normal human skin bind monomeric IgE via Fc epsilon RI. J Exp Med. 1992 May 1;175(5):1353–1365. doi: 10.1084/jem.175.5.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Watts C., Lanzavecchia A. Suppressive effect of antibody on processing of T cell epitopes. J Exp Med. 1993 Oct 1;178(4):1459–1463. doi: 10.1084/jem.178.4.1459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Yamaguchi M., Lantz C. S., Oettgen H. C., Katona I. M., Fleming T., Miyajima I., Kinet J. P., Galli S. J. IgE enhances mouse mast cell Fc(epsilon)RI expression in vitro and in vivo: evidence for a novel amplification mechanism in IgE-dependent reactions. J Exp Med. 1997 Feb 17;185(4):663–672. doi: 10.1084/jem.185.4.663. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Immunology are provided here courtesy of British Society for Immunology

RESOURCES