Home LiteratureArticle Details
PMID: 7561694 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Successful T cell priming in B cell-deficient mice.

The Journal of experimental medicine ·Vol. 182 ·No. 4 ·1995-10-01 ·Pages 915-22

Epstein MM, Di Rosa F, Jankovic D, Sher A, Matzinger P

Abstract

B cells are an abundant population of lymphocytes that can efficiently capture, process, and present antigen for recognition by activated or memory T cells. Controversial experiments and arguments exist, however, as to whether B cells are or should be involved in the priming of virgin T cells in vivo. Using B cell-deficient mice, we have studied the role of B cells as antigen-presenting cells in a wide variety of tests, including assays of T cell proliferation and cytokine production in responses to protein antigens, T cell killing to minor and major histocompatibility antigens, skin graft rejection, and the in vitro and in vivo responses to shistosome eggs. We found that B cells are not critical for either CD4 or CD8 T cell priming in any of these systems. This finding lends support to the notion that the priming of T cells is reserved for specialized cells such as dendritic cells and that antigen presentation by B cells serves distinct immunological functions.

MeSH Terms
Animals Antigen Presentation Antigen-Presenting Cells/immunology B-Lymphocytes/immunology CD4-Positive T-Lymphocytes/immunology CD8-Positive T-Lymphocytes/immunology Cytokines/analysis Female Fluorescent Antibody Technique Immunoglobulin mu-Chains/genetics Lymphocyte Activation Male Mice Mice, Inbred C57BL Mice, Mutant Strains Schistosomiasis mansoni/immunology Skin Transplantation T-Lymphocytes/immunology
Chemicals
Cytokines Immunoglobulin mu-Chains
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Epstein M M
Laboratory of Cellular and Molecular Immunology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland 20892, USA.
Di Rosa F
Jankovic D
Sher A
Matzinger P
References (71)
71 references, click to expand
  1. The JAM test. A simple assay for DNA fragmentation and cell death.
    J Immunol Methods. 1991 Dec 15;145(1-2):185-92 PMID: 1765650
  2. Small B cells as antigen-presenting cells in the induction of tolerance to soluble protein antigens.
    J Exp Med. 1992 Jan 1;175(1):131-8 PMID: 1730913
  3. CD4+ Th2 response induced by Schistosoma mansoni eggs develops rapidly, through an early, transient, Th0-like stage.
    J Immunol. 1992 Apr 1;148(7):2283-90 PMID: 1347553
  4. 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):223-41 PMID: 3155791
  5. Antigen-specific interaction between T and B cells.
    Nature. 1985 Apr 11-17;314(6011):537-9 PMID: 3157869
  6. Production of a monoclonal antibody to and molecular characterization of B-cell stimulatory factor-1.
    Nature. 1985 May 23-29;315(6017):333-6 PMID: 2582266
  7. Antigen-specific B cells efficiently present low doses of antigen for induction of T cell proliferation.
    J Immunol. 1985 Aug;135(2):980-8 PMID: 2409164
  8. 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):2937-45 PMID: 2413104
  9. T cell development in B cell-deficient mice. IV. The role of B cells as antigen-presenting cells in vivo.
    J Immunol. 1986 Feb 1;136(3):823-9 PMID: 2416835
  10. Capacity of B cells to function as stimulators of a primary mixed leukocyte reaction.
    J Immunol. 1986 Nov 15;137(10):3117-23 PMID: 2945857
  11. Normal rejection of xenografts by strongly deficient B-cell animals (X-linked immunodeficient mice).
    Transplant Proc. 1992 Apr;24(2):494 PMID: 1566401
  12. Cellular basis of skin allograft rejection: an in vivo model of immune-mediated tissue destruction.
    Annu Rev Immunol. 1992;10:333-58 PMID: 1590990
  13. Germinal centers and antibody production in bone marrow.
    Immunol Rev. 1992 Apr;126:99-112 PMID: 1597323
  14. A fail-safe mechanism for maintaining self-tolerance.
    J Exp Med. 1992 Aug 1;176(2):553-64 PMID: 1386876
  15. B cells turn off virgin but not memory T cells.
    Science. 1992 Nov 13;258(5085):1156-9 PMID: 1439825
  16. B lymphocytes in vivo fail to prime naive T cells but can stimulate antigen-experienced T lymphocytes.
    J Exp Med. 1993 Mar 1;177(3):679-90 PMID: 8436906
  17. "Infectious" transplantation tolerance.
    Science. 1993 Feb 12;259(5097):974-7 PMID: 8094901
  18. Analysis of cytokine mRNA expression during primary granuloma formation induced by eggs of Schistosoma mansoni.
    J Immunol. 1993 Aug 1;151(3):1430-40 PMID: 8335939
  19. Altered response of CD4+ T cell subsets to Plasmodium chabaudi chabaudi in B cell-deficient mice.
    Int Immunol. 1993 Oct;5(10):1343-8 PMID: 8268139
  20. Tolerogenicity of resting and activated B cells.
    J Exp Med. 1994 Jan 1;179(1):249-58 PMID: 7505799
  21. Indirect recognition by helper cells can induce donor-specific cytotoxic T lymphocytes in vivo.
    J Exp Med. 1994 Mar 1;179(3):865-72 PMID: 8113680
  22. Induction of B cell and T cell tolerance in vivo by anti-CD23 mAb.
    J Immunol. 1994 Apr 15;152(8):3768-76 PMID: 8144946
  23. In vivo activation of naive T cells by antigen-presenting B cells.
    J Immunol. 1994 Apr 15;152(8):3777-85 PMID: 8144947
  24. Immunology. Memories are made of this?
    Nature. 1994 Jun 23;369(6482):605-6 PMID: 8208285
  25. Tolerance, danger, and the extended family.
    Annu Rev Immunol. 1994;12:991-1045 PMID: 8011301
  26. IL-12 inhibits Th2 cytokine responses induced by eggs of Schistosoma mansoni.
    J Immunol. 1994 Aug 15;153(4):1707-13 PMID: 7913944
  27. Host response to eggs of S. mansoni. I. Granuloma formation in the unsensitized laboratory mouse.
    Am J Pathol. 1962 Dec;41:711-31 PMID: 13930476
  28. Demonstration of MHC-specific haemolytic plaque-forming cells.
    Nature. 1979 Mar 29;278(5703):449-51 PMID: 377088
  29. Characterization of a monoclonal antibody directed against mouse macrophage and lymphocyte Fc receptors.
    J Exp Med. 1979 Sep 19;150(3):580-96 PMID: 90108
  30. Hybridoma cell lines secreting monoclonal antibodies to mouse H-2 and Ia antigens.
    J Immunol. 1980 Feb;124(2):533-40 PMID: 7188699
  31. Xenogeneic monoclonal antibodies to mouse lymphoid differentiation antigens.
    Immunol Rev. 1979;47:63-90 PMID: 398327
  32. Studies on the capacity of B cells to serve as antigen-presenting cells.
    J Immunol. 1981 Mar;126(3):1075-9 PMID: 6970212
  33. B220: a B cell-specific member of th T200 glycoprotein family.
    Nature. 1981 Feb 19;289(5799):681-3 PMID: 6970340
  34. B-cell suppression by anti-IgM antibody: humoral and cellular analyses.
    Cell Immunol. 1981 Jul 1;61(2):404-15 PMID: 6788381
  35. A shared alloantigenic determinant on Ia antigens encoded by the I-A and I-E subregions: evidence for I region gene duplication.
    J Immunol. 1981 Dec;127(6):2488-95 PMID: 6170707
  36. A monoclonal antibody discriminating between subsets of T and B cells.
    J Immunol. 1981 Dec;127(6):2496-501 PMID: 6975326
  37. Major histocompatibility complex-restricted antigen presentation to antigen-reactive T cells by B lymphocyte tumor cells.
    J Exp Med. 1981 Nov 1;154(5):1419-31 PMID: 6170720
  38. A monoclonal antibody specific for mouse dendritic cells.
    Proc Natl Acad Sci U S A. 1982 Jan;79(1):161-5 PMID: 6948298
  39. Defective induction of antigen-reactive proliferating T cells in B cell-deprived mice.
    Eur J Immunol. 1981 Dec;11(12):964-8 PMID: 6173237
  40. Flow cytometry as an analytical and preparative tool in immunology.
    J Immunol Methods. 1982;50(3):R85-112 PMID: 7047643
  41. B cells as antigen-presenting cells: the requirement for B cell activation.
    J Immunol. 1983 Jul;131(1):109-14 PMID: 6190900
  42. Characterization of the murine antigenic determinant, designated L3T4a, recognized by monoclonal antibody GK1.5: expression of L3T4a by functional T cell clones appears to correlate primarily with class II MHC antigen-reactivity.
    Immunol Rev. 1983;74:29-56 PMID: 6195085
  43. Cutaneous leishmaniasis in anti-IgM-treated mice: enhanced resistance due to functional depletion of a B cell-dependent T cell involved in the suppressor pathway.
    J Immunol. 1984 Apr;132(4):2072-7 PMID: 6230400
  44. 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 PMID: 6607969
  45. Antigen presentation by hapten-specific B lymphocytes. I. Role of surface immunoglobulin receptors.
    J Exp Med. 1984 Oct 1;160(4):1102-13 PMID: 6207262
  46. Resting and sensitized T lymphocytes exhibit distinct stimulatory (antigen-presenting cell) requirements for growth and lymphokine release.
    J Exp Med. 1984 Dec 1;160(6):1717-35 PMID: 6239901
  47. Capacity of small B cell-enriched populations to stimulate mixed lymphocyte reactions: marked differences between irradiated vs. mitomycin C-treated stimulators.
    Eur J Immunol. 1985 Jan;15(1):92-6 PMID: 3155688
  48. The B cell is the initiating antigen-presenting cell in peripheral lymph nodes.
    J Immunol. 1987 Feb 15;138(4):1051-5 PMID: 3100626
  49. Antigen presentation by hapten-specific B lymphocytes. IV. Comparative ability of B cells to present specific antigen and anti-immunoglobulin antibody.
    J Immunol. 1987 May 1;138(9):2822-5 PMID: 3494773
  50. T cell priming in vivo: a major role for B cells in presenting antigen to T cells in lymph nodes.
    J Immunol. 1987 May 1;138(9):2848-56 PMID: 2952725
  51. Studies in experimental eosinophilia. V. Eosinophils in lynph nodes of guinea pigs following primary antigenic stimulation.
    Am J Pathol. 1963 May;42:529-49 PMID: 13930964
  52. Granuloma formation around Schistosoma mansoni, S. HAEMATOBIUM, AND S. japonicum eggs. Size and rate of development, cellular composition, cross-sensitivity, and rate of egg destruction.
    Am J Trop Med Hyg. 1970 Mar;19(2):292-304 PMID: 5462634
  53. Effect of anti-immunoglobulin antisera on homograft rejection in mice.
    Nat New Biol. 1972 May 10;237(71):58-9 PMID: 4555684
  54. Towards a network theory of the immune system.
    Ann Immunol (Paris). 1974 Jan;125C(1-2):373-89 PMID: 4142565
  55. Responsiveness to HY antigen Ir gene complementation and target cell specificity.
    Immunol Rev. 1977;35:59-75 PMID: 70400
  56. Major histocompatibility complex-linked immune-responsiveness is acquired by lymphocytes of low-responder mice differentiating in thymus of high-responder mice.
    Proc Natl Acad Sci U S A. 1978 May;75(5):2439-42 PMID: 307765
  57. Monoclonal xenogeneic antibodies to murine cell surface antigens: identification of novel leukocyte differentiation antigens.
    Eur J Immunol. 1978 Aug;8(8):539-51 PMID: 81133
  58. The role of antigen-presenting B cells in T cell priming in vivo. Studies of B cell-deficient mice.
    J Immunol. 1988 Jun 1;140(11):3773-8 PMID: 2453554
  59. Can B cells turn on virgin T cells?
    Nature. 1988 Jul 21;334(6179):253-5 PMID: 2969460
  60. Regulation of antigen-presentation-I. IFN-gamma induces antigen-presenting properties on B cells.
    J Immunol. 1988 Dec 15;141(12):4083-8 PMID: 2974053
  61. Distinct features of dendritic cells and anti-Ig activated B cells as stimulators of the primary mixed leukocyte reaction.
    J Exp Med. 1989 Jan 1;169(1):239-54 PMID: 2562848
  62. B-lymphoma cells process and present their endogenous immunoglobulin to major histocompatibility complex-restricted T cells.
    Proc Natl Acad Sci U S A. 1989 Jan;86(1):282-6 PMID: 2492101
  63. Induction of classical transplantation tolerance in the adult.
    J Exp Med. 1989 Mar 1;169(3):779-94 PMID: 2647894
  64. Interleukin 5 is required for the blood and tissue eosinophilia but not granuloma formation induced by infection with Schistosoma mansoni.
    Proc Natl Acad Sci U S A. 1990 Jan;87(1):61-5 PMID: 2104985
  65. Do small B cells induce tolerance?
    Transplant Proc. 1991 Feb;23(1 Pt 1):729-30 PMID: 1990666
  66. Egg deposition is the major stimulus for the production of Th2 cytokines in murine schistosomiasis mansoni.
    J Immunol. 1991 Feb 15;146(4):1322-7 PMID: 1825109
  67. Murine Th1 and Th2 clones proliferate optimally in response to distinct antigen-presenting cell populations.
    J Immunol. 1991 Mar 15;146(6):1750-8 PMID: 1826010
  68. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene.
    Nature. 1991 Apr 4;350(6317):423-6 PMID: 1901381
  69. Novel pathways of antigen presentation for the maintenance of memory.
    Int Immunol. 1991 Feb;3(2):141-8 PMID: 2025614
  70. Microbial induction of co-stimulatory activity for CD4 T-cell growth.
    Int Immunol. 1991 Apr;3(4):323-32 PMID: 1831651
  71. Strong priming of T cells adoptively transferred into scid mice.
    J Exp Med. 1991 Dec 1;174(6):1653-6 PMID: 1744589
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
1995-10-01
Pages
915-22
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2192294
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: product@genelibs.com