Immunoproteasome inhibition induces plasma cell apoptosis and preserves kidney allografts by activating the unfolded protein response and suppressing plasma cell survival factors

Kidney Int. 2019 Mar;95(3):611-623. doi: 10.1016/j.kint.2018.10.022. Epub 2019 Jan 23.

Abstract

Chronic antibody-mediated rejection is the leading cause of allograft dysfunction and loss after kidney transplantation, and current immunosuppressive regimens fail to target the plasma cells that produce alloantibodies. We previously showed that treatment with the immunoproteasome inhibitor ONX 0914 prevented the expansion of plasma cells and prevented chronic allograft nephropathy and organ failure after kidney transplantation in rats, but the mechanism has remained elusive. In the current study, we confirmed a long-term reduction in alloantibody production and improvements in allograft histology in rats treated with ONX 0914 or with the broad-spectrum proteasome inhibitor bortezomib. Plasma cells from allotransplanted rats expressed immunoproteasomes at high levels. Immunoproteasome inhibition with ONX 0914 led to ubiquitin-conjugate accumulation, activation of the unfolded protein response, and induction of apoptosis in plasma cells. In addition, ONX 0914 suppressed the expression of adhesion molecules (VLA-4 and LFA-1), plasma cell survival factors (APRIL and IL-6), and IFN-γ-inducible chemokines in bone marrow, while the APRIL receptor BCMA, the IL-6 receptor, and the chemokine receptors CXCR4 and CXCR3 were down-regulated on plasma cells. Taken together, immunoproteasome inhibition blocked alloantibody production by inducing apoptosis of plasma cells through activating the unfolded protein response and suppressing plasma cell survival factors in the bone marrow.

Keywords: chronic rejection; immunoproteasome; kidney transplantation; plasma cell; survival niche; unfolded protein response.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Allografts / drug effects
  • Allografts / immunology
  • Animals
  • Apoptosis / drug effects
  • Apoptosis / immunology
  • Bortezomib / pharmacology
  • Bortezomib / therapeutic use
  • Cell Survival / drug effects
  • Cell Survival / immunology
  • Disease Models, Animal
  • Graft Rejection / immunology
  • Graft Rejection / prevention & control*
  • Humans
  • Isoantibodies / immunology
  • Isoantibodies / metabolism
  • Kidney / drug effects
  • Kidney / immunology
  • Kidney Transplantation / adverse effects*
  • Male
  • Oligopeptides / pharmacology
  • Oligopeptides / therapeutic use
  • Plasma Cells / drug effects*
  • Plasma Cells / immunology
  • Proteasome Endopeptidase Complex / immunology*
  • Proteasome Endopeptidase Complex / metabolism
  • Proteasome Inhibitors / pharmacology*
  • Proteasome Inhibitors / therapeutic use
  • Rats
  • Rats, Inbred F344
  • Rats, Inbred Lew
  • Transplantation, Homologous
  • Unfolded Protein Response / drug effects
  • Unfolded Protein Response / immunology

Substances

  • Isoantibodies
  • Oligopeptides
  • PR-957
  • Proteasome Inhibitors
  • Bortezomib
  • Proteasome Endopeptidase Complex