Small Molecule Inhibition of Rab7 Impairs B Cell Class Switching and Plasma Cell Survival To Dampen the Autoantibody Response in Murine Lupus

J Immunol. 2016 Nov 15;197(10):3792-3805. doi: 10.4049/jimmunol.1601427. Epub 2016 Oct 14.

Abstract

IgG autoantibodies mediate pathology in systemic lupus patients and lupus-prone mice. In this study, we showed that the class-switched IgG autoantibody response in MRL/Faslpr/lpr and C57/Sle1Sle2Sle2 mice was blocked by the CID 1067700 compound, which specifically targeted Ras-related in brain 7 (Rab7), an endosome-localized small GTPase that was upregulated in activated human and mouse lupus B cells, leading to prevention of disease development and extension of lifespan. These were associated with decreased IgG-expressing B cells and plasma cells, but unchanged numbers and functions of myeloid cells and T cells. The Rab7 inhibitor suppressed T cell-dependent and T cell-independent Ab responses, but it did not affect T cell-mediated clearance of Chlamydia infection, consistent with a B cell-specific role of Rab7. Indeed, B cells and plasma cells were inherently sensitive to Rab7 gene knockout or Rab7 activity inhibition in class switching and survival, respectively, whereas proliferation/survival of B cells and generation of plasma cells were not affected. Impairment of NF-κB activation upon Rab7 inhibition, together with the rescue of B cell class switching and plasma cell survival by enforced NF-κB activation, indicated that Rab7 mediates these processes by promoting NF-κB activation, likely through signal transduction on intracellular membrane structures. Thus, a single Rab7-inhibiting small molecule can target two stages of B cell differentiation to dampen the pathogenic autoantibody response in lupus.

MeSH terms

  • Animals
  • Autoantibodies / immunology*
  • B-Lymphocytes / drug effects
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / physiology
  • Cell Proliferation / drug effects
  • Cell Survival
  • Chlamydia Infections / immunology
  • Female
  • Gene Expression Regulation
  • Heterocyclic Compounds, 2-Ring / pharmacology*
  • Immunoglobulin Class Switching / drug effects*
  • Immunoglobulin G / genetics
  • Immunoglobulin G / immunology
  • Lupus Erythematosus, Systemic / immunology*
  • Lupus Erythematosus, Systemic / physiopathology
  • Lymphocyte Activation
  • Mice
  • Mice, Inbred MRL lpr
  • NF-kappa B / drug effects
  • NF-kappa B / metabolism
  • Plasma Cells / drug effects
  • Plasma Cells / immunology
  • Plasma Cells / physiology*
  • T-Lymphocytes / immunology
  • Thiourea / analogs & derivatives*
  • Thiourea / pharmacology
  • Up-Regulation
  • rab GTP-Binding Proteins / antagonists & inhibitors*
  • rab GTP-Binding Proteins / genetics
  • rab GTP-Binding Proteins / immunology
  • rab7 GTP-Binding Proteins

Substances

  • Autoantibodies
  • CID1067700
  • Heterocyclic Compounds, 2-Ring
  • Immunoglobulin G
  • NF-kappa B
  • rab7 GTP-Binding Proteins
  • rab7 GTP-binding proteins, human
  • rab7 GTP-binding proteins, mouse
  • rab GTP-Binding Proteins
  • Thiourea