The role of B lymphocytes as antigen-presenting cells

Archivum Immunologiae et Therapiae Experimentalis

Volumn 56, Issue 2, 2008, Pages 77-83

  Chen, Xinjian ^a   Jensen, Peter E ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Antigen presentation; B lymphocytes; HLA DO; Regulatory T cells

Indexed keywords

ANTIBODY; AUTOANTIBODY; B LYMPHOCYTE ANTIGEN; B LYMPHOCYTE RECEPTOR; EPITOPE; HLA DO ANTIGEN;

ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL FUNCTION; DISSOCIATION; HUMAN; LYMPHOCYTE DIFFERENTIATION; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE;

ANIMALS; ANTIGEN PRESENTATION; ANTIGEN-PRESENTING CELLS; B-LYMPHOCYTES; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; LYMPHOCYTE ACTIVATION;

EID: 42349090206     PISSN: 0004069X     EISSN: 16614917     Source Type: Journal    
DOI: 10.1007/s00005-008-0014-5     Document Type: Review

References (72)

1. Akiba H., Oshima H., Takeda K., Atsuta M., Nakano H., Nakajima A., Nohara C., Yagita H. and Okumura K. (1999): CD28-independent costimulation of T cells by OX40 ligand and CD70 on activated B cells. J. Immunol., 162, 7058-7066.
2. Al-Alwan M. M., Okkenhaug K., Vanhaesebroeck B., Hayflick J. S. and Marshall A. J. (2007): Requirement for phosphoinositide 3-kinase p110delta signaling in B cell antigen receptor-mediated antigen presentation. J. Immunol., 178, 2328-2335.
3. Ashwell J. D. (1988): Are B lymphocytes the principal antigen-presenting cells in vivo? J. Immunol., 140, 3697-3700.
4. Ashwell J. D., DeFranco A. L., Paul W. E. and Schwartz R. H. (1984): Antigen presentation by resting B cells. Radiosensitivity of the antigen-presentation function and two distinct pathways of T cell activation. J. Exp. Med., 159, 881-905.
5. Boackle S. A., Morris M. A., Holers V. M. and Karp D. R. (1998): Complement opsonization is required for presentation of immune complexes by resting peripheral blood B cells. J. Immunol., 161, 6537-6543.
6. Braley-Mullen H. and Yu S. (2000): Early requirement for B cells for development of spontaneous autoimmune thyroiditis in NOD.H-2h4 mice. J. Immunol., 165, 7262-7269.
7. Brown B. K. and Song W. (2001): The actin cytoskeleton is required for the trafficking of the B cell antigen receptor to the late endosomes. Traffic, 2, 414-427.
8. Byersdorfer C. A., Dipaolo R. J., Petzold S. J. and Unanue E. R. (2004): Following immunization antigen becomes concentrated in a limited number of APCs including B cells. J. Immunol., 173, 6627-6634.
9. Campbell K. S. (1999): Signal transduction from the B cell antigen-receptor. Curr. Opin. Immunol., 11, 256-264.
10. Chan O. T., Hannum L. G., Haberman A. M., Madaio M. P. and Shlomchik M. J. (1999): A novel mouse with B cells but lacking serum antibody reveals an antibody-independent role for B cells in murine lupus. J. Exp. Med., 189, 1639-1648.
11. Chen C., Rivera A., Ron N., Dougherty J. P. and Ron Y. (2001): A gene therapy approach for treating T-cell-mediated autoimmune diseases. Blood, 97, 886-894.
12. Chen C. C., Rivera A., Dougherty J. P. and Ron Y. (2004): Complete protection from relapsing experimental autoimmune encephalomyelitis induced by syngeneic B cells expressing the autoantigen. Blood, 103, 4616-4618.
13. Chen X. and Jensen P. E. (2004): The expression of HLA-DO (H2-O) in B lymphocytes. Immunol. Res., 29, 19-28.
14. Chen X. and Jensen P. E. (2007): Cutting edge: primary B lymphocytes preferentially expand allogeneic FoxP3+ CD4 T cells. J. Immunol., 179, 2046-2050.
15. Chen X., Laur O., Kambayashi T., Li S., Bray R. A., Weber D. A., Karlsson L. and Jensen P. E. (2002): Regulated expression of human histocompatibility leukocyte antigen (HLA)-DO during antigen-dependent and antigen-independent phases of B cell development. J. Exp. Med., 195, 1053-1062.
16. Cheng P. C., Steele C. R., Gu L., Song W. and Pierce S. K. (1999): MHC class II antigen processing in B cells: accelerated intracellular targeting of antigens. J. Immunol., 162, 7171-7180.
17. Chicz R. M., Urban R. G., Gorga J. C., Vignali D. A., Lane W. S. and Strominger J. L. (1993): Specificity and promiscuity among naturally processed peptides bound to HLA-DR alleles. J. Exp. Med., 178, 27-47.
18. Clark M. R., Massenburg D., Zhang M. and Siemasko K. (2003): Molecular mechanisms of B cell antigen receptor trafficking. Ann. NY Acad. Sci., 987, 26-37.
19. Constant S. L. (1999): B lymphocytes as antigen-presenting cells for CD4+ T cell priming in vivo. J. Immunol., 162, 5695-5703.
20. Crawford A., Macleod M., Schumacher T., Corlett L. and Gray D. (2006): Primary T cell expansion and differentiation in vivo requires antigen presentation by B cells. J. Immunol., 176, 3498-3506.
21. Deretic V. (2006): Autophagy as an immune defense mechanism. Curr. Opin. Immunol., 18, 375-382.
22. Ding L. and Shevach E. M. (1996): Activated B cells express CD28/B7-independent costimulatory activity. J. Immunol., 157, 1389-1396.
23. Dongre A. R., Kovats S., deRoos P., McCormack A. L., Nakagawa T., Paharkova-Vatchkova V., Eng J., Caldwell H., Yates J. R. 3rd and Rudensky A. Y. (2001): In vivo MHC class II presentation of cytosolic proteins revealed by rapid automated tandem mass spectrometry and functional analyses. Eur. J. Immunol., 31, 1485-1494.
24. Drake L., McGovern-Brindisi E. M. and Drake J. R. (2006): BCR ubiquitination controls BCR-mediated antigen processing and presentation. Blood, 108, 4086-4093.
25. Epstein M. M., Di Rosa F., Jankovic D., Sher A. and Matzinger P. (1995): Successful T cell priming in B cell-deficient mice. J. Exp. Med., 182, 915-922.
26. Eynon E. E. and Parker D. C. (1992): Small B cells as antigen-presenting cells in the induction of tolerance to soluble protein antigens. J. Exp. Med., 175, 131-138.
27. Fallas J. L., Tobin H. M., Lou O., Guo D., Sant'Angelo D. B. and Denzin L. K. (2004): Ectopic expression of HLA-DO in mouse dendritic cells diminishes MHC class II antigen presentation. J. Immunol., 173, 1549-1560.
28. Fuchs E. J. and Matzinger P. (1992): B cells turn off virgin but not memory T cells. Science, 258, 1156-1159.
29. Garside P., Ingulli E., Merica R. R., Johnson J. G., Noelle R. J. and Jenkins M. K. (1998): Visualization of specific B and T lymphocyte interactions in the lymph node. Science, 281, 96-99.
30. Glazier K. S., Hake S. B., Tobin H. M., Chadburn A., Schattner E. J. and Denzin L. K. (2002): Germinal center B cells regulate their capability to present antigen by modulation of HLA-DO. J. Exp. Med., 195, 1063-1069.
31. Gondre-Lewis T. A., Moquin A. E. and Drake J. R. (2001): Prolonged antigen persistence within nonterminal late endocytic compartments of antigen-specific B lymphocytes. J. Immunol., 166, 6657-6664.
32. Granboulan M., Lankar D., Raposo G., Bonnerot C. and Hivroz C. (2003): Phosphoinositide 3-kinase activation by Igbeta controls de novo formation of an antigen-processing compartment. J. Biol. Chem., 278, 4331-4338.
33. Hayglass K. T., Naides S. J., Scott C. F. Jr., Benacerraf B. and Sy M. S. (1986): T cell development in B cell-deficient mice. IV. The role of B cells as antigen-presenting cells in vivo. J. Immunol., 136, 823-829.
34. Janeway C. A. Jr., Ron J. and Katz M. E. (1987): The B cell is the initiating antigen-presenting cell in peripheral lymph nodes. J. Immunol., 138, 1051-1055.
35. Kim Y. M., Pan J. Y., Korbel G. A., Peperzak V., Boes M. and Ploegh H. L. (2006): Monovalent ligation of the B cell receptor induces receptor activation but fails to promote antigen presentation. Proc. Natl. Acad. Sci. USA, 103, 3327-3332.
36. Kropshofer H., Vogt A. B., Thery C., Armandola E. A., Li B. C., Moldenhauer G., Amigorena S. and Hammerling G. J. (1998): A role for HLA-DO as a co-chaperone of HLA-DM in peptide loading of MHC class II molecules. EMBO J., 17, 2971-2981.
37. Kurt-Jones E. A., Liano D., HayGlass K. A., Benacerraf B., Sy M. S. and Abbas A. K. (1988): The role of antigen-presenting B cells in T cell priming in vivo. Studies of B cell-deficient mice. J. Immunol., 140, 3773-3778.
38. Langhorne J., Cross C., Seixas E., Li C. and von der Weid T. (1998): A role for B cells in the development of T cell helper function in a malaria infection in mice. Proc. Natl. Acad. Sci. USA, 95, 1730-1734.
39. Lankar D., Vincent-Schneider H., Briken V., Yokozeki T., Raposo G. and Bonnerot C. (2002): Dynamics of major histocompatibility complex class II compartments during B cell receptor-mediated cell activation. J. Exp. Med., 195, 461-472.
40. Lanzavecchia A. (1985): Antigen-specific interaction between T and B cells. Nature, 314, 537-539.
41. Lanzavecchia A. (1987): Antigen uptake and accumulation in antigen-specific B cells. Immunol. Rev., 99, 39-51.
42. Lanzavecchia A. (1990): Receptor-mediated antigen uptake and its effect on antigen presentation to class II-restricted T lymphocytes. Annu. Rev. Immunol., 8, 773-793.
43. Lin R. H., Mamula M. J., Hardin J. A. and Janeway C. A. Jr. (1991): Induction of autoreactive B cells allows priming of autoreactive T cells. J. Exp. Med., 173, 1433-1439.
44. Linton P. J., Harbertson J. and Bradley L. M. (2000): A critical role for B cells in the development of memory CD4 cells. J. Immunol., 165, 5558-5565.
45. Liu Y. J. and Arpin C. (1997): Germinal center development. Immunol. Rev., 156, 111-126.
46. Lund F. E., Hollifield M., Schuer K., Lines J. L., Randall T. D. and Garvy B. A. (2006): B cells are required for generation of protective effector and memory CD4 cells in response to Pneumocystis lung infection. J. Immunol., 176, 6147-6154.
47. Macaulay A. E., DeKruyff R. H. and Umetsu D. T. (1998): Antigen-primed T cells from B cell-deficient JHD mice fail to provide B cell help. J. Immunol., 160, 1694-1700.
48. Madsen L., Labrecque N., Engberg J., Dierich A., Svejgaard A., Benoist C., Mathis D. and Fugger L. (1999): Mice lacking all conventional MHC class II genes. Proc. Natl. Acad. Sci. USA, 96, 10338-10343.
49. Malkiel S., Factor S. and Diamond B. (1999): Autoimmune myocarditis does not require B cells for antigen presentation. J. Immunol., 163, 5265-5268.
50. Mann M. K., Maresz K., Shriver L. P., Tan Y. and Dittel B. N. (2007): B cell regulation of CD4+CD25+ T regulatory cells and IL-10 via B7 is essential for recovery from experimental autoimmune encephalomyelitis. J. Immunol., 178, 3447-3456.
51. Muntasell A., Carrascal M., Alvarez I., Serradell L., van Veelen P., Verreck F. A., Koning F., Abian J. and Jaraquemada D. (2004): Dissection of the HLA-DR4 peptide repertoire in endocrine epithelial cells: strong influence of invariant chain and HLA-DM expression on the nature of ligands. J. Immunol., 173, 1085-1093.
52. Nashar T. O. and Drake J. R. (2005): The pathway of antigen uptake and processing dictates MHC class II-mediated B cell survival and activation. J. Immunol., 174, 1306-1316.
53. Oxenius A., Campbell K. A., Maliszewski C. R., Kishimoto T., Kikutani H., Hengartner H., Zinkernagel R. M. and Bachmann M. F. (1996): CD40-CD40 ligand interactions are critical in T-B cooperation but not for other anti-viral CD4+ T cell functions. J. Exp. Med., 183, 2209-2218.
54. Pape K. A., Catron D. M., Itano A. A. and Jenkins M. K. (2007): The humoral immune response is initiated in lymph nodes by B cells that acquire soluble antigen directly in the follicles. Immunity, 26, 491-502.
55. Parekh V. V., Prasad D. V., Banerjee P. P., Joshi B. N., Kumar A. and Mishra G. C. (2003): B cells activated by lipopolysaccharide, but not by anti-Ig and anti-CD40 antibody, induce anergy in CD8+ T cells: role of TGF-beta 1. J. Immunol., 170, 5897-5911.
56. Parker D. C. (1993): T cell-dependent B cell activation. Annu. Rev. Immunol., 11, 331-360.
57. Phillips J. A., Romball C. G., Hobbs M. V., Ernst D. N., Shultz L. and Weigle W. O. (1996): CD4+ T cell activation and tolerance induction in B cell knockout mice. J. Exp. Med., 183, 1339-1344.
58. Reichardt P., Dornbach B., Rong S., Beissert S., Gueler F., Loser K. and Gunzer M. (2007): Naive B cells generate regulatory T cells in the presence of a mature immunologic synapse. Blood, 110, 1519-1529.
59. Reith W. and Mach B. (2001): The bare lymphocyte syndrome and the regulation of MHC expression. Annu. Rev. Immunol., 19, 331-373.
60. Ron Y. and Sprent J. (1987): T cell priming in vivo: a major role for B cells in presenting antigen to T cells in lymph nodes. J. Immunol., 138, 2848-2856.
61. Ronchese F. and Hausmann B. (1993): B lymphocytes in vivo fail to prime naive T cells but can stimulate antigen-experienced T lymphocytes. J. Exp. Med., 177, 679-690.
62. Rowe V., Banovic T., MacDonald K. P., Kuns R., Don A. L., Morris E. S., Burman A. C., Bofinger H. M., Clouston A. D. and Hill G. R. (2006): Host B cells produce IL-10 following TBI and attenuate acute GVHD after allogeneic bone marrow transplantation. Blood, 108, 2485-2492.
63. Schmid D. and Munz C. (2007): Innate and adaptive immunity through autophagy. Immunity, 27, 11-21.
64. Seamons A., Perchellet A. and Goverman J. (2006): Endogenous myelin basic protein is presented in the periphery by both dendritic cells and resting B cells with different functional consequences. J. Immunol., 177, 2097-2106.
65. Siemasko K., Eisfelder B. J., Williamson E., Kabak S. and Clark M. R. (1998): Cutting edge: signals from the B lymphocyte antigen receptor regulate MHC class II containing late endosomes. J. Immunol., 160, 5203-5208.
66. Sunshine G. H., Jimmo B. L., Ianelli C. and Jarvis L. (1991): Strong priming of T cells adoptively transferred into SCID mice. J. Exp. Med., 174, 1653-1656.
67. Topham D. J., Tripp R. A., Hamilton-Easton A. M., Sarawar S. R. and Doherty P. C. (1996): Quantitative analysis of the influenza virus-specific CD4+ T cell memory in the absence of B cells and Ig. J. Immunol., 157, 2947-2952.
68. Vascotto F., Lankar D., Faure-Andre G., Vargas P., Diaz J., Le Roux D., Yuseff M. I., Sibarita J. B., Boes M., Raposo G., Mougneau E., Glaichenhaus N., Bonnerot C., Manoury B. and Lennon-Dumenil A. M. (2007): The actin-based motor protein myosin II regulates MHC class II trafficking and BCR-driven antigen presentation. J. Cell Biol., 176, 1007-1019.
69. Werner-Klein M., Dresch C., Marconi P. and Brocker T. (2007): Transcriptional targeting of B cells for induction of peripheral CD8 T cell tolerance. J. Immunol., 178, 7738-7746.
70. Wolf S. D., Dittel B. N., Hardardottir F. and Janeway C. A. Jr. (1996): Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. J. Exp. Med., 184, 2271-2278.
71. Yan J., Harvey B. P., Gee R. J., Shlomchik M. J. and Mamula M. J. (2006): B cells drive early T cell autoimmunity in vivo prior to dendritic cell-mediated autoantigen presentation. J. Immunol., 177, 4481-4487.
72. Zhong G., Reis e Sousa C. and Germain R. N. (1997): Antigen-unspecific B cells and lymphoid dendritic cells both show extensive surface expression of processed antigen-major histocompatibility complex class II complexes after soluble protein exposure in vivo or in vitro. J. Exp. Med., 186, 673-682.