Inhibition of lipopolysaccharide-induced osteoclast formation and bone resorption in vitro and in vivo by cysteine proteinase inhibitors

J Leukoc Biol. 2017 May;101(5):1233-1243. doi: 10.1189/jlb.3A1016-433R. Epub 2017 Feb 14.

Abstract

Inflammation-induced bone destruction is a major treatment target in many inflammatory skeletal diseases. The aim of this study was to investigate if the cysteine proteinase inhibitors cystatin C, fungal cysteine proteinase inhibitor (E-64), and N-benzyloxycarbonyl-arginyl-leucyl-valyl-glycyl-diazomethane acetate (Z-RLVG-CHN2) can inhibit LPS-induced osteoclast formation. Mouse bone marrow macrophages (BMMs) were isolated and primed with receptor activator of NF-κB ligand (RANKL) for 24 h, followed by stimulation with LPS, with and without inhibitors. Adult mice were injected locally with LPS and then treated with E-64 and osteoclast formation assessed by the number of cathepsin K+ multinucleated cells. Cystatin C inhibited LPS-induced osteoclast formation time and concentration dependently (IC50 = 0.3 μM). The effect was associated with decreased mRNA and protein expression of tartrate-resistant acid phosphatase (TRAP) and cathepsin K and of the osteoclastogenic transcription factors c-Fos and NFATc1. LPS-induced osteoclast formation on bone slices was also inhibited by cystatin C, resulting in decreased pit formation and release of bone matrix proteins. Similar data were obtained with E-64 and Z-RLVG-CHN2 Cystatin C was internalized in BMMs stimulated by LPS but not in unstimulated BMMs. Osteoclast formation induced by LPS was dependent on TNF-α, and the 3 inhibitors abolished LPS-induced TNF superfamily 2 (gene encoding TNF-α; Tnfsf2) mRNA expression without affecting Il1b, Il6, or oncostatin M (Osm) expression. Formation of osteoclasts in the skull bones after local LPS stimulation was inhibited by E-64. It is concluded that cysteine proteinase inhibitors effectively inhibit LPS-induced osteoclast formation in vivo and in vitro by inhibition of TNF-α expression. The targeting of cysteine proteinases might represent a novel treatment modality for prevention of inflammatory bone loss.

Keywords: cystatin C; inflammation; macrophages; periodontitis; rheumatoid arthritis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bone Density Conservation Agents / pharmacology*
  • Bone Marrow Cells / drug effects
  • Bone Marrow Cells / immunology
  • Bone Marrow Cells / pathology
  • Bone Resorption / chemically induced
  • Bone Resorption / genetics
  • Bone Resorption / immunology
  • Bone Resorption / prevention & control*
  • Cathepsin K / genetics
  • Cathepsin K / immunology
  • Cystatin C / pharmacology*
  • Cysteine Proteinase Inhibitors / pharmacology*
  • Dose-Response Relationship, Immunologic
  • Gene Expression Regulation
  • Interleukin-6 / genetics
  • Interleukin-6 / immunology
  • Leucine / analogs & derivatives*
  • Leucine / pharmacology
  • Lipopolysaccharides / antagonists & inhibitors
  • Lipopolysaccharides / pharmacology
  • Macrophages / drug effects
  • Macrophages / immunology
  • Macrophages / pathology
  • Mice
  • NFATC Transcription Factors / genetics
  • NFATC Transcription Factors / immunology
  • Oligopeptides / pharmacology*
  • Oncostatin M / genetics
  • Oncostatin M / immunology
  • Osteoclasts / drug effects*
  • Osteoclasts / immunology
  • Osteoclasts / pathology
  • Primary Cell Culture
  • Proto-Oncogene Proteins c-fos / genetics
  • Proto-Oncogene Proteins c-fos / immunology
  • RANK Ligand / antagonists & inhibitors
  • RANK Ligand / pharmacology
  • Signal Transduction
  • Tartrate-Resistant Acid Phosphatase / genetics
  • Tartrate-Resistant Acid Phosphatase / immunology
  • Tumor Necrosis Factor-alpha / antagonists & inhibitors
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / immunology

Substances

  • Bone Density Conservation Agents
  • Cystatin C
  • Cysteine Proteinase Inhibitors
  • Interleukin-6
  • Lipopolysaccharides
  • NFATC Transcription Factors
  • Nfatc1 protein, mouse
  • Oligopeptides
  • Proto-Oncogene Proteins c-fos
  • RANK Ligand
  • Tnfsf11 protein, mouse
  • Tumor Necrosis Factor-alpha
  • interleukin-6, mouse
  • Oncostatin M
  • Acp5 protein, mouse
  • Tartrate-Resistant Acid Phosphatase
  • Cathepsin K
  • Ctsk protein, mouse
  • Leucine
  • E 64