Major Histocompatibility Complex Class II Presentation of Cell-associated Antigen is Mediated by CD8alpha+ Dendritic Cells in Vivo

Overview

Journal J Exp Med

Specialties Allergy & Immunology
General Medicine

Date 2002 Mar 20

PMID 11901195

Citations 22

Authors

Yanet Valdez

Weiling Mah

Monte M Winslow

Lixin Xu

Peter Ling

Sarah E Townsend

Affiliations

Soon will be listed here.

Abstract

Antigen-specific B cells express major histocompatibility complex class II and can present antigen directly to T cells. Adoptive transfer experiments using transgenic B and T cells demonstrated that antigen-specific B cells can also efficiently transfer antigen to another cell for presentation to T cells in vivo. To identify the antigen-presenting cell that receives antigens from B cells, a strategy was developed to follow the traffic of B cell-derived proteins in vivo. B cells were labeled with the fluorescent dye CFSE and loaded with antigen, before adoptive transfer into recipient mice. Populations of splenocytes from the recipient mice were later assayed for the presence of fluorescent proteins and for the ability to activate T cells. A small number of CD8alpha+CD4-CD11b(lo) dendritic cells (DCs) contain proteins transferred from B cells and these DCs effectively present antigens derived from the B cells to T cells. The results suggest that CD8alpha+ DCs sample the cells and membranes in their environment for presentation to T cells circulating through the T cell zone. This function of CD8alpha+ DCs may be relevant to the priming of an immune response or the induction of T cell tolerance.

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References

Huang J, Yang Y, Sepulveda H, Shi W, Hwang I, Peterson P . TCR-Mediated internalization of peptide-MHC complexes acquired by T cells. Science. 1999; 286(5441):952-4. DOI: 10.1126/science.286.5441.952. View

Hawiger D, Inaba K, Dorsett Y, Guo M, Mahnke K, Rivera M . Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J Exp Med. 2001; 194(6):769-79. PMC: 2195961. DOI: 10.1084/jem.194.6.769. View

Gallucci S, Lolkema M, Matzinger P . Natural adjuvants: endogenous activators of dendritic cells. Nat Med. 1999; 5(11):1249-55. DOI: 10.1038/15200. View

Peterson D, DIPAOLO R, Kanagawa O, UNANUE E . Quantitative analysis of the T cell repertoire that escapes negative selection. Immunity. 1999; 11(4):453-62. DOI: 10.1016/s1074-7613(00)80120-x. View

Heijnen H, Schiel A, Fijnheer R, Geuze H, Sixma J . Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood. 1999; 94(11):3791-9. View

Steinman R, Turley S, Mellman I, Inaba K . The induction of tolerance by dendritic cells that have captured apoptotic cells. J Exp Med. 2000; 191(3):411-6. PMC: 2195815. DOI: 10.1084/jem.191.3.411. View

Brasel K, De Smedt T, Smith J, Maliszewski C . Generation of murine dendritic cells from flt3-ligand-supplemented bone marrow cultures. Blood. 2000; 96(9):3029-39. View

den Haan J, Lehar S, Bevan M . CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J Exp Med. 2000; 192(12):1685-96. PMC: 2213493. DOI: 10.1084/jem.192.12.1685. View

Albert M, Sauter B, Bhardwaj N . Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature. 1998; 392(6671):86-9. DOI: 10.1038/32183. View

10.

Banchereau J, Steinman R . Dendritic cells and the control of immunity. Nature. 1998; 392(6673):245-52. DOI: 10.1038/32588. View

11.

Bevan M . 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; 143(5):1283-8. PMC: 2190184. DOI: 10.1084/jem.143.5.1283. View

12.

Rock K, Benacerraf B, Abbas A . Antigen presentation by hapten-specific B lymphocytes. I. Role of surface immunoglobulin receptors. J Exp Med. 1984; 160(4):1102-13. PMC: 2187484. DOI: 10.1084/jem.160.4.1102. View

13.

Goodnow C, Crosbie J, Adelstein S, Lavoie T, Brink R, Wotherspoon J . Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature. 1988; 334(6184):676-82. DOI: 10.1038/334676a0. View

14.

Strasser A, Whittingham S, Vaux D, Bath M, Adams J, Cory S . Enforced BCL2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc Natl Acad Sci U S A. 1991; 88(19):8661-5. PMC: 52569. DOI: 10.1073/pnas.88.19.8661. View

15.

Germain R, Margulies D . The biochemistry and cell biology of antigen processing and presentation. Annu Rev Immunol. 1993; 11:403-50. DOI: 10.1146/annurev.iy.11.040193.002155. View

16.

Cooke M, Heath A, Shokat K, Zeng Y, Finkelman F, Linsley P . Immunoglobulin signal transduction guides the specificity of B cell-T cell interactions and is blocked in tolerant self-reactive B cells. J Exp Med. 1994; 179(2):425-38. PMC: 2191355. DOI: 10.1084/jem.179.2.425. View

17.

Ho W, Cooke M, Goodnow C, Davis M . Resting and anergic B cells are defective in CD28-dependent costimulation of naive CD4+ T cells. J Exp Med. 1994; 179(5):1539-49. PMC: 2191488. DOI: 10.1084/jem.179.5.1539. View

18.

Lyons A, Parish C . Determination of lymphocyte division by flow cytometry. J Immunol Methods. 1994; 171(1):131-7. DOI: 10.1016/0022-1759(94)90236-4. View

19.

Cyster J, Hartley S, Goodnow C . Competition for follicular niches excludes self-reactive cells from the recirculating B-cell repertoire. Nature. 1994; 371(6496):389-95. DOI: 10.1038/371389a0. View

20.

Cyster J, Goodnow C . Antigen-induced exclusion from follicles and anergy are separate and complementary processes that influence peripheral B cell fate. Immunity. 1995; 3(6):691-701. DOI: 10.1016/1074-7613(95)90059-4. View