Novel Effects of Combination Therapy Through Inhibition of Caspase-1/Gasdermin D Induced-Pyroptosis in Lupus Nephritis

Front Immunol. 2021 Nov 19:12:720877. doi: 10.3389/fimmu.2021.720877. eCollection 2021.

Abstract

Objectives: Combination therapy with mycophenolate mofetil, tacrolimus and steroids are effective in achieving complete remission in lupus nephritis (LN). Combination therapy uniquely downregulated caspase-1 compared with monotherapies, which can cleave gasdermin D (GSDMD) and was recently identified as the pyroptosis executioner. We therefore investigated whether combination therapy enabled the suppression of caspase-1/GSDMD-mediated pyroptosis in LN.

Methods: Expression and activation of GSDMD were detected in kidney specimens of the human and mouse with LN using immunohistochemical staining and immunoblotting. Primary podocytes isolated from MRL/lpr mice were incubated with LPS+ATP, and pretreated with monotherapy or combination therapy. Inhibition of caspase-1/GSDMD-induced pyroptosis by combination therapy were assessed in MRL/lpr mice and human specimens. Pyroptosis was examined using a FAM caspase-1 kit and flow cytometry. The correlation between pyroptosis in peripheral blood and the systemic lupus erythematosus disease activity index (SLEDAI) was analyzed.

Results: Kidney tissue specimens from LN patients and mice exhibited greatly increased expression levels and cleavage of GSDMD. In cultured podocytes, combination treatment significantly suppressed the activation of NLRP3 and caspase-1 and reduced GSDMD N-terminal levels. Combination therapy repressed disease progression through inhibition of caspase-1/GSDMD-mediated pyroptosis in both humans and MRL/lpr mice. Caspase-1/PI positive cell numbers in peripheral blood were positively correlated with SLE-DAI. LN patients with complete remission and partial remission had remarkably reduced caspase-1/PI positive cell numbers compared to baseline. Ac-FLTD-CMK, a GSDMD-derived inhibitor, prevented the development of LN.

Conclusion: Combination therapy suppressed caspase-1/GSDMD-mediated pyroptosis in vitro and in vivo and reduced disease progression.

Keywords: caspase-1; gasdermin D; lupus nephritis; pyroptosis; therapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Animals
  • Calcineurin Inhibitors / administration & dosage
  • Caspase 1 / drug effects
  • Caspase Inhibitors / administration & dosage*
  • Cells, Cultured
  • Cohort Studies
  • Disease Models, Animal
  • Drug Therapy, Combination
  • Female
  • Humans
  • Intracellular Signaling Peptides and Proteins / antagonists & inhibitors*
  • Kidney / drug effects
  • Kidney / metabolism
  • Kidney / pathology
  • Lupus Nephritis / drug therapy*
  • Lupus Nephritis / metabolism
  • Lupus Nephritis / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Inbred MRL lpr
  • Middle Aged
  • Mycophenolic Acid / administration & dosage
  • Phosphate-Binding Proteins / antagonists & inhibitors*
  • Podocytes / drug effects
  • Podocytes / metabolism
  • Podocytes / pathology
  • Prednisone / administration & dosage
  • Pyroptosis / drug effects
  • Tacrolimus / administration & dosage
  • Young Adult

Substances

  • Calcineurin Inhibitors
  • Caspase Inhibitors
  • GSDMD protein, human
  • Gsdmd protein, mouse
  • Intracellular Signaling Peptides and Proteins
  • Phosphate-Binding Proteins
  • Casp1 protein, mouse
  • Caspase 1
  • Mycophenolic Acid
  • Prednisone
  • Tacrolimus