B lymphocytes acquire and present intracellular antigens that have relocated to the surface of apoptotic target cells

European Journal of Immunology

Volumn 41, Issue 7, 2011, Pages 1850-1861

  Ciechomska, Marzena ^a   Lennard, Thomas W J ^a   Kirby, John A ^a   Knight, Andrew M ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Antigen processing and presentation; Apoptosis; B cell; CD4+ T cell; Relocation

Indexed keywords

ANTIGEN; CHIMERIC PROTEIN; CHIMERIC PROTEIN E T; TETANUS TOXIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FEMALE; HELA CELL; HUMAN; HUMAN CELL; IMMUNITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGEN PRESENTATION; ANTIGEN-PRESENTING CELLS; ANTIGENS, SURFACE; APOPTOSIS; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; CELL MEMBRANE; FLOW CYTOMETRY; HELA CELLS; HUMANS; LYMPHOCYTE ACTIVATION; MICE; PEPTIDE FRAGMENTS; TETANUS TOXIN;

EID: 79959747286     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201141472     Document Type: Article

References (42)

1. Chen, X. and Jensen, P. E., The role of B lymphocytes as antigen-presenting cells. Arch. Immunol. Ther. Exp. (Warsz). 2008. 56: 77-83.
2. Rock, K. L., Benacerraf, B. and Abbas, A. K., Antigen presentation by hapten-specific B lymphocytes. I. Role of surface immunoglobulin receptors. J. Exp. Med. 1984. 160: 1102-1113.
3. Lanzavecchia, A., Antigen-specific interaction between T and B cells. Nature 1985. 314: 537-539.
4. Stockinger, B., Zal, T., Zal, A. and Gray, D., B cells solicit their own help from T cells. J. Exp. Med. 1996. 183: 891-899.
5. Lund, F. E., Cytokine-producing B lymphocytes-key regulators of immunity. Curr. Opin. Immunol. 2008. 20: 332-338.
6. Pape, K. A., Catron, D. M., Itano, A. A. and Jenkins, M. K., The humoral immune response is initiated in lymph nodes by B cells that acquire soluble antigen directly in the follicles. Immunity 2007. 26: 491-502.
7. Roozendaal, R., Mempel, T. R., Pitcher, L. A., Gonzalez, S. F., Verschoor, A., Mebius, R. E., von Andrian, U. H. and Carroll, M. C., Conduits mediate transport of low-molecular-weight antigen to lymph node follicles. Immunity 2009. 30: 264-276.
8. Szakal, A. K., Gieringer, R. L., Kosco, M. H. and Tew, J. G., Isolated follicular dendritic cells: cytochemical antigen localization, Nomarski, SEM, and TEM morphology. J. Immunol. 1985. 134: 1349-1359.
9. Batista, F. D. and Neuberger, M. S., B cells extract and present immobilized antigen: implications for affinity discrimination. EMBO J. 2000. 19: 513-520.
10. Batista, F. D., Iber, D. and Neuberger, M. S., B cells acquire antigen from target cells after synapse formation. Nature 2001. 411: 489-494.
11. Puaux, A. L., Campanaud, J., Salles, A., Preville, X., Timmerman, B., Joly, E. and Hudrisier, D., A very rapid and simple assay based on trogocytosis to detect and measure specific T and B cell reactivity by flow cytometry. Eur. J. Immunol. 2006. 36: 779-788.
12. Carrasco, Y. R. and Batista, F. D., B cells acquire particulate antigen in a macrophage-rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity 2007. 27: 160-171.
13. Junt, T., Moseman, E. A., Iannacone, M., Massberg, S., Lang, P. A., Boes, M., Fink, K. et al., Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 2007. 450: 110-114.
14. Phan, T. G., Grigorova, I., Okada, T. and Cyster, J. G., Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat. Immunol. 2007. 8: 992-1000.
15. Kosco, M. H., Szakal, A. K. and Tew, J. G., In vivo obtained antigen presented by germinal center B cells to T cells in vitro. J. Immunol. 1988. 140: 354-360.
16. Wykes, M., Pombo, A., Jenkins, C. and MacPherson, G. G., Dendritic cells interact directly with naive B lymphocytes to transfer antigen and initiate class switching in a primary T-dependent response. J. Immunol. 1998. 161: 1313-1319.
17. Rodriguez-Pinto, D., B cells as antigen presenting cells. Cell Immunol. 2005. 238: 67-75.
18. Tesniere, A., Panaretakis, T., Kepp, O., Apetoh, L., Ghiringhelli, F., Zitvogel, L. and Kroemer, G., Molecular characteristics of immunogenic cancer cell death. Cell Death Differ. 2008. 15: 3-12.
19. Fairweather, N. F. and Lyness, V. A., The complete nucleotide sequence of tetanus toxin. Nucleic Acids Res. 1986. 14: 7809-7812.
20. Patterson, G. H., Knobel, S. M., Sharif, W. D., Kain, S. R. and Piston, D. W., Use of the green fluorescent protein and its mutants in quantitative fluorescence microscopy. Biophys. J. 1997. 73: 2782-2790.
21. Hewitt, E. W., Treumann, A., Morrice, N., Tatnell, P. J., Kay, J. and Watts, C., Natural processing sites for human cathepsin E and cathepsin D in tetanus toxin: implications for T cell epitope generation. J. Immunol. 1997. 159: 4693-4699.
22. Obeid, M., Tesniere, A., Ghiringhelli, F., Fimia, G. M., Apetoh, L., Perfettini, J. L., Castedo, M. et al., Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med. 2007. 13: 54-61.
23. Batista, F. D. and Harwood, N. E., The who, how and where of antigen presentation to B cells. Nat. Rev. Immunol. 2009. 9: 15-27.
24. Qin, D., Wu, J., Vora, K. A., Ravetch, J. V., Szakal, A. K., Manser, T. and Tew, J. G., Fc gamma receptor IIB on follicular dendritic cells regulates the B cell recall response. J. Immunol. 2000. 164: 6268-6275.
25. Fang, Y., Xu, C., Fu, Y. X., Holers, V. M. and Molina, H., Expression of complement receptors 1 and 2 on follicular dendritic cells is necessary for the generation of a strong antigen-specific IgG response. J. Immunol. 1998. 160: 5273-5279.
26. Gray, D., Kosco, M. and Stockinger, B., Novel pathways of antigen presentation for the maintenance of memory. Int. Immunol. 1991. 3: 141-148.
27. Delamarre, L., Pack, M., Chang, H., Mellman, I. and Trombetta, E. S., Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 2005. 307: 1630-1634.
28. Bergtold, A., Desai, D. D., Gavhane, A. and Clynes, R., Cell surface recycling of internalized antigen permits dendritic cell priming of B cells. Immunity 2005. 23: 503-514.
29. Diao, J., Winter, E., Chen, W., Xu, F. and Cattral, M. S., Antigen transmission by replicating antigen-bearing dendritic cells. J. Immunol. 2007. 179: 2713-2721.
30. Nzula, S., Going, J. J. and Stott, D. I., Antigen-driven clonal proliferation, somatic hypermutation, and selection of B lymphocytes infiltrating human ductal breast carcinomas. Cancer Res. 2003. 63: 3275-3280.
31. Willis, S. N., Mallozzi, S. S., Rodig, S. J., Cronk, K. M., McArdel, S. L., Caron, T., Pinkus, G. S. et al., The microenvironment of germ cell tumors harbors a prominent antigen-driven humoral response. J. Immunol. 2009. 182: 3310-3317.
32. Hansen, M. H., Nielsen, H. and Ditzel, H. J., The tumor-infiltrating B cell response in medullary breast cancer is oligoclonal and directed against the autoantigen actin exposed on the surface of apoptotic cancer cells. Proc. Natl. Acad. Sci. USA 2001. 98: 12659-12664.
33. Hansen, M. H., Nielsen, H. V. and Ditzel, H. J., Translocation of an intracellular antigen to the surface of medullary breast cancer cells early in apoptosis allows for an antigen-driven antibody response elicited by tumor-infiltrating B cells. J. Immunol. 2002. 169: 2701-2711.
34. Panaretakis, T., Joza, N., Modjtahedi, N., Tesniere, A., Vitale, I., Durchschlag, M., Fimia, G. M. et al., The co-translocation of ERp57 and calreticulin determines the immunogenicity of cell death. Cell Death Differ. 2008. 15: 1499-1509.
35. Obeid, M., Panaretakis, T., Joza, N., Tufi, R., Tesniere, A., van Endert, P., Zitvogel, L. and Kroemer, G., Calreticulin exposure is required for the immunogenicity of gamma-irradiation and UVC light-induced apoptosis. Cell Death Differ. 2007. 14: 1848-1850.
36. Panaretakis, T., Kepp, O., Brockmeier, U., Tesniere, A., Bjorklund, A. C., Chapman, D. C., Durchschlag, M. et al., Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. EMBO J. 2009. 28: 578-590.
37. Gray, M., Miles, K., Salter, D., Gray, D. and Savill, J., Apoptotic cells protect mice from autoimmune inflammation by the induction of regulatory B cells. Proc. Natl. Acad. Sci. USA 2007. 104: 14080-14085.
38. Kim, K. J., Kanellopoulos-Langevin, C., Merwin, R. M., Sachs, D. H. and Asofsky, R., Establishment and characterization of BALB/c lymphoma lines with B cell properties. J. Immunol. 1979. 122: 549-554.
39. Knight, A. M., Lucocq, J. M., Prescott, A. R., Ponnambalam, S. and Watts, C., Antigen endocytosis and presentation mediated by human membrane IgG1 in the absence of the Ig(alpha)/Ig(beta) dimer. EMBO J. 1997. 16: 3842-3850.
40. White, J., Blackman, M., Bill, J., Kappler, J., Marrack, P., Gold, D. P. and Born, W., Two better cell lines for making hybridomas expressing specific T cell receptors. J. Immunol. 1989. 143: 1822-1825.
41. Antoniou, A. N. and Watts, C., Antibody modulation of antigen presentation: positive and negative effects on presentation of the tetanus toxin antigen via the murine B cell isoform of FcgammaRII. Eur. J. Immunol. 2002. 32: 530-540.
42. Gillis, S. and Smith, K. A., Long term culture of tumour-specific cytotoxic T cells. Nature 1977. 268: 154-156.