Suppression of RANKL-dependent heme oxygenase-1 is required for high mobility group box 1 release and osteoclastogenesis

J Cell Biochem. 2012 Feb;113(2):486-98. doi: 10.1002/jcb.23372.

Abstract

The differentiation of osteoclasts is regulated by several essential cytokines, such as receptor activator of nuclear factor κB ligand (RANKL) and macrophage colony-stimulating factor. Recently, high mobility group box 1 (HMGB1), a chromatin protein, also has been identified as one of these osteoclast differentiation cytokines. However, the molecular mechanisms that control HMGB1 release from osteoclast precursor cells are not known. Here, we report that RANKL-induced suppression of heme oxygenase-1 (HO-1), a heme-degrading enzyme, promotes HMGB1 release during osteoclastogenesis. In contrast, induction of HO-1 with hemin or curcumin in bone marrow-derived macrophages or RAW-D murine osteoclast precursor cells inhibited osteoclastogenesis and suppressed HMGB1 release. Since an inhibitor for p38 mitogen-activated protein kinase (MAPK) prevented the RANKL-mediated HO-1 suppression and extracellular release of HMGB1, these effects were p38 MAPK-dependent. Moreover, suppression of HO-1 in RAW-D cells by RNA interference promoted the activation of caspase-3 and HMGB1 release, whereas overexpression of HO-1 inhibited caspase-3 activation as well as HMGB1 release. Furthermore, these effects were regulated by redox conditions since antioxidant N-acetylcysteine abolished the HO-1/HMGB1/caspase-3 axis. These results suggest that RANKL-dependent HO-1 suppression leads to caspase-3 activation and HMGB1 release during osteoclastogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acid Phosphatase / metabolism
  • Animals
  • Bilirubin / pharmacology
  • Caspase 3 / metabolism
  • Cell Differentiation / drug effects*
  • Cell Proliferation
  • Cells, Cultured
  • Curcumin / pharmacology
  • Enzyme Activation
  • Gene Expression Regulation / drug effects
  • HMGB1 Protein / metabolism*
  • Heme Oxygenase-1 / genetics
  • Heme Oxygenase-1 / metabolism*
  • Hemin / pharmacology
  • Isoenzymes / metabolism
  • MAP Kinase Signaling System
  • Macrophage Colony-Stimulating Factor / pharmacology
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Macrophages / physiology
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Organometallic Compounds / pharmacology
  • Osteoclasts / drug effects
  • Osteoclasts / metabolism
  • Osteoclasts / physiology*
  • RANK Ligand / pharmacology*
  • RANK Ligand / physiology
  • Reactive Oxygen Species / metabolism
  • Tartrate-Resistant Acid Phosphatase

Substances

  • HMGB1 Protein
  • Isoenzymes
  • Organometallic Compounds
  • RANK Ligand
  • Reactive Oxygen Species
  • Tnfsf11 protein, mouse
  • tricarbonyldichlororuthenium (II) dimer
  • Hemin
  • Macrophage Colony-Stimulating Factor
  • Heme Oxygenase-1
  • Acid Phosphatase
  • Tartrate-Resistant Acid Phosphatase
  • Casp3 protein, mouse
  • Caspase 3
  • Curcumin
  • Bilirubin