B lymphocytes treated in vitro with antigen coupled to cholera toxin B subunit induce antigen-specific Foxp3(+) regulatory T cells and protect against experimental autoimmune encephalomyelitis

J Immunol. 2012 Feb 15;188(4):1686-97. doi: 10.4049/jimmunol.1101771. Epub 2012 Jan 16.

Abstract

The ability of activated B cells to protect against various experimental autoimmune or allergic diseases makes them attractive for use in cell-based therapies. We describe an efficient way to generate B cells with strong suppressive functions by incubating naive B cells with a relevant Ag conjugated to cholera toxin B subunit (CTB). This allows most B cells, irrespective of BCR, to take up and present Ag and induces their expression of latency-associated polypeptide (LAP)/TGF-β and after adoptive transfer also their production of IL-10. With OVA as model Ag, when naive T cells were cocultured in vitro with B cells pretreated with OVA conjugated to CTB (OVA/CTB) Ag-specific CD4(+) Foxp3 regulatory T (Treg) cells increased >50-fold. These cells effectively suppressed CD25(-)CD4(+) effector T (Teff) cells in secondary cultures. Adoptive transfer of OVA/CTB-treated B cells to mice subsequently immunized with OVA in CFA induced increase in Foxp3 Treg cells together with suppression and depletion of Teff cells. Likewise, adoptive transfer of B cells pulsed with myelin oligodendrocyte glycoprotein peptide(35-55) (MOGp) conjugated to CTB increased the number of Treg cells, suppressed MOGp-specific T cell proliferation and IL-17 and IFN-γ production, and prevented the development of experimental autoimmune encephalomyelitis. Similar effects were seen when B cells were given "therapeutically" to mice with early-stage experimental autoimmune encephalomyelitis. Our results suggest that B cells pulsed in vitro with relevant Ag/CTB conjugates may be used in cell therapy to induce Ag-specific suppression of autoimmune disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adoptive Transfer / methods
  • Animals
  • Antigens / immunology*
  • B-Lymphocytes* / drug effects
  • B-Lymphocytes* / immunology
  • B-Lymphocytes* / metabolism
  • CD4-Positive T-Lymphocytes / immunology
  • Cell Proliferation / drug effects
  • Cholera Toxin / administration & dosage
  • Cholera Toxin / immunology*
  • Encephalomyelitis, Autoimmune, Experimental / immunology*
  • Female
  • Forkhead Transcription Factors / analysis
  • Glycoproteins / immunology
  • Immune Tolerance
  • Interferon-gamma / biosynthesis
  • Interleukin-17 / biosynthesis
  • Interleukin-17 / immunology
  • Lymphocyte Activation / immunology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Myelin-Oligodendrocyte Glycoprotein
  • Ovalbumin / immunology
  • Ovalbumin / pharmacology
  • Peptide Fragments / immunology
  • Recombinant Fusion Proteins
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / metabolism

Substances

  • Antigens
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Glycoproteins
  • Interleukin-17
  • Myelin-Oligodendrocyte Glycoprotein
  • Peptide Fragments
  • Recombinant Fusion Proteins
  • myelin oligodendrocyte glycoprotein (35-55)
  • Interferon-gamma
  • Ovalbumin
  • Cholera Toxin