Exposure of a distinct PDCA-1+ (CD317) B cell population to agonistic anti-4-1BB (CD137) inhibits T and B cell responses both in vitro and in vivo

PLoS One. 2012;7(11):e50272. doi: 10.1371/journal.pone.0050272. Epub 2012 Nov 21.

Abstract

4-1BB (CD137) is an important T cell activating molecule. Here we report that it also promotes development of a distinct B cell subpopulation co-expressing PDCA-1. 4-1BB is expressed constitutively, and its expression is increased when PDCA-1(+) B cells are activated. We found that despite a high level of surface expression of 4-1BB on PDCA-1(+) B cells, treatment of these cells with agonistic anti-4-1BB mAb stimulated the expression of only a few activation markers (B7-2, MHC II, PD-L2), cytokines (IL-12p40/p70), and chemokines (MCP-1, RANTES), as well as sTNFR1, and the immunosuppressive enzyme, IDO. Although the PDCA-1(+) B cells stimulated by anti-4-1BB expressed MHC II at high levels and took up antigens efficiently, Ig class switching was inhibited when they were pulsed with T-independent (TI) or T-dependent (TD) Ags and adoptively transferred into syngeneic recipients. Furthermore, when anti-4-1BB-treated PDCA-1(+) B cells were pulsed with OVA peptide and combined with Vα2(+)CD4(+) T cells, Ag-specific cell division was inhibited both in vitro and in vivo. Our findings suggest that the 4-1BB signal transforms PDCA-1(+) B cells into propagators of negative immune regulation, and establish an important role for 4-1BB in PDCA-1(+) B cell development and function.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adoptive Transfer
  • Animals
  • Antibodies, Monoclonal / pharmacology*
  • B-Lymphocytes / cytology
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / metabolism
  • Bone Marrow Cells / immunology
  • Cell Division / drug effects
  • Cell Division / immunology
  • Cell Lineage
  • Cytokines / biosynthesis
  • Cytokines / immunology
  • Gene Expression / drug effects
  • Gene Expression / immunology
  • Histocompatibility Antigens Class II / genetics
  • Histocompatibility Antigens Class II / immunology
  • Immunoglobulin Class Switching / drug effects
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / genetics
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / immunology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Ovalbumin / pharmacology
  • Protein Isoforms / genetics
  • Protein Isoforms / immunology
  • T-Lymphocytes / cytology
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism
  • Tumor Necrosis Factor Receptor Superfamily, Member 9 / genetics*
  • Tumor Necrosis Factor Receptor Superfamily, Member 9 / immunology

Substances

  • Antibodies, Monoclonal
  • Cytokines
  • Histocompatibility Antigens Class II
  • Indoleamine-Pyrrole 2,3,-Dioxygenase
  • Protein Isoforms
  • Tumor Necrosis Factor Receptor Superfamily, Member 9
  • Ovalbumin

Grants and funding

This study was supported by grants from the National Cancer Center, Korea (NCC1210370-1 and NCC1130720-1) and the National Research Foundation of Korea (NRF2005-0093837 and NRF2006-2004212). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.