The RP105/MD-1 complex is indispensable for TLR4/MD-2-dependent proliferation and IgM-secreting plasma cell differentiation of marginal zone B cells

Int Immunol. 2012 Jun;24(6):389-400. doi: 10.1093/intimm/dxs040. Epub 2012 Feb 21.

Abstract

Marginal zone (MZ) B cells mount rapid T-cell-independent (T-I) immune responses against microbial components such as LPS. While Toll-like receptor 4 (TLR4) is essential for LPS responses, MZ B cells uniquely express high levels of another LPS sensor Radioprotective 105 (RP105). However, little is known about how RP105 is used by MZ B cells. In this study, we investigated TLR4- or RP105-dependent MZ B cell responses by utilizing agonistic monoclonal antibodies (mAbs) to each receptor. Cross-linking TLR4 and RP105 at the same time with the mAbs induced robust IgM-secreting plasma cell generation as lipid A moiety of LPS. In contrast, stimulation with either mAb alone did not elicit such responses. RP105-deficient MZ B cells failed to produce IgM-secreting plasma cells in response to lipid A. TLR4 or lipid A stimulation of MZ B cells up-regulated their B lymphocyte-induced maturation protein 1 (Blimp-1) and X-box-binding protein 1 (Xbp-1) mRNA expression. RP105 stimulation alone did not give these responses and in fact decreased TLR4-mediated their expression. Compared with wild-type (WT) MZ B cells, RP105-deficient MZ B cells exhibited increased levels of Blimp-1 and Xbp-1 mRNA expression in response to lipid A. Lipid A or TLR4 plus RP105 stimulation induced massive proliferation and expression of Bcl-xL and c-Myc in WT but not RP105-deficient MZ B cells. These responses contributed to TLR4-mediated anti-apoptotic responses in MZ B cells. Thus, RP105 contributes in a unique way to the TLR4-dependent survival, proliferation and plasma cell generation of MZ B cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies / immunology
  • Antibodies / pharmacology
  • Antigens, CD / genetics
  • Antigens, CD / immunology*
  • Antigens, CD / metabolism
  • Antigens, Surface / genetics
  • Antigens, Surface / immunology*
  • Antigens, Surface / metabolism
  • B-Lymphocytes / drug effects
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / metabolism
  • Blotting, Western
  • Cell Differentiation / drug effects
  • Cell Differentiation / immunology
  • Cell Proliferation
  • Cells, Cultured
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / immunology
  • DNA-Binding Proteins / metabolism
  • Flow Cytometry
  • Gene Expression
  • Immunoglobulin M / immunology
  • Immunoglobulin M / metabolism
  • Lipid A / pharmacology
  • Lymphocyte Antigen 96 / genetics
  • Lymphocyte Antigen 96 / immunology*
  • Lymphocyte Antigen 96 / metabolism
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / immunology*
  • Membrane Glycoproteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Multiprotein Complexes / genetics
  • Multiprotein Complexes / immunology
  • Multiprotein Complexes / metabolism
  • Plasma Cells / drug effects
  • Plasma Cells / immunology*
  • Plasma Cells / metabolism
  • Positive Regulatory Domain I-Binding Factor 1
  • Proto-Oncogene Proteins c-myc / immunology
  • Proto-Oncogene Proteins c-myc / metabolism
  • Regulatory Factor X Transcription Factors
  • Reverse Transcriptase Polymerase Chain Reaction
  • Toll-Like Receptor 4 / genetics
  • Toll-Like Receptor 4 / immunology*
  • Toll-Like Receptor 4 / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / immunology
  • Transcription Factors / metabolism
  • X-Box Binding Protein 1
  • bcl-X Protein / immunology
  • bcl-X Protein / metabolism

Substances

  • Antibodies
  • Antigens, CD
  • Antigens, Surface
  • Bcl2l1 protein, mouse
  • DNA-Binding Proteins
  • Immunoglobulin M
  • Lipid A
  • Ly78 protein, mouse
  • Ly86 protein, mouse
  • Ly96 protein, mouse
  • Lymphocyte Antigen 96
  • Membrane Glycoproteins
  • Multiprotein Complexes
  • Myc protein, mouse
  • Prdm1 protein, mouse
  • Proto-Oncogene Proteins c-myc
  • Regulatory Factor X Transcription Factors
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • Transcription Factors
  • X-Box Binding Protein 1
  • Xbp1 protein, mouse
  • bcl-X Protein
  • Positive Regulatory Domain I-Binding Factor 1