Enhanced osteoclastogenesis by mitochondrial retrograde signaling through transcriptional activation of the cathepsin K gene

Ann N Y Acad Sci. 2016 Jan;1364(1):52-61. doi: 10.1111/nyas.12709. Epub 2015 Mar 18.

Abstract

Mitochondrial dysfunction has emerged as an important factor in wide ranging human pathologies. We have previously defined a retrograde signaling pathway that originates from dysfunctional mitochondria (Mt-RS) and causes a global nuclear transcriptional reprograming as its end point. Mitochondrial dysfunction causing disruption of mitochondrial membrane potential and consequent increase in cytosolic calcium [Ca(2) ](c) activates calcineurin and the transcription factors NF-κB, NFAT, CREB, and C/EBPδ. In macrophages, this signaling complements receptor activator of nuclear factor kappa-B ligand (RANKL)-induced osteoclastic differentiation. Here, we show that the Mt-RS activated transcriptional coactivator heterogeneous ribonucleoprotein A2 (hnRNP A2) is induced by hypoxia in murine macrophages. We demonstrate that the cathepsin K gene (Ctsk), one of the key genes upregulated during osteoclast differentiation, is transcriptionally activated by Mt-RS factors. HnRNP A2 acts as a coactivator with nuclear transcription factors, cRel, and C/EBPδ for Ctsk promoter activation under hypoxic conditions. Notably, our study shows that hypoxia-induced activation of the stress target factors mediates effects similar to that of RANKL with regard to Ctsk activation. We therefore suggest that mitochondrial dysfunction and activation of Mt-RS, induced by various pathophysiologic conditions, is a potential risk factor for osteoclastogenesis and bone loss.

Keywords: Ctsk promoter; Guha, M., S. Srinivasan, A. Koenigstein, M. Zaidi & N.G. Avadhani. 2015. Enhanced osteoclastogenesis by mitochond-rial retrograde signaling through transcriptional activation of the cathepsin K gene. In “MARROW,” ed. by M. Zaidi. Ann. N.Y. Acad. Sci.; hnRNP A2; hypoxia; mitochondrial retrograde signaling; osteoclastogenesis.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CCAAT-Enhancer-Binding Protein-delta / antagonists & inhibitors
  • CCAAT-Enhancer-Binding Protein-delta / genetics
  • CCAAT-Enhancer-Binding Protein-delta / metabolism
  • Cathepsin K / antagonists & inhibitors
  • Cathepsin K / chemistry
  • Cathepsin K / genetics
  • Cathepsin K / metabolism*
  • Cell Hypoxia
  • Cyclic AMP Response Element-Binding Protein / antagonists & inhibitors
  • Cyclic AMP Response Element-Binding Protein / genetics
  • Cyclic AMP Response Element-Binding Protein / metabolism
  • Genes, Reporter
  • Heterogeneous-Nuclear Ribonucleoprotein Group A-B / antagonists & inhibitors
  • Heterogeneous-Nuclear Ribonucleoprotein Group A-B / genetics
  • Heterogeneous-Nuclear Ribonucleoprotein Group A-B / metabolism
  • Mice
  • Mitochondria / enzymology
  • Mitochondria / metabolism*
  • NFATC Transcription Factors / antagonists & inhibitors
  • NFATC Transcription Factors / genetics
  • NFATC Transcription Factors / metabolism
  • Osteoclasts / cytology
  • Osteoclasts / enzymology
  • Osteoclasts / metabolism*
  • Osteogenesis*
  • Promoter Regions, Genetic*
  • RANK Ligand / metabolism
  • RAW 264.7 Cells
  • RNA Interference
  • RNA, Messenger / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Signal Transduction*
  • Transcriptional Activation

Substances

  • Cebpd protein, mouse
  • Creb1 protein, mouse
  • Cyclic AMP Response Element-Binding Protein
  • Heterogeneous-Nuclear Ribonucleoprotein Group A-B
  • NFATC Transcription Factors
  • Nfatc1 protein, mouse
  • RANK Ligand
  • RNA, Messenger
  • Recombinant Proteins
  • Tnfsf11 protein, mouse
  • hnRNP A2
  • CCAAT-Enhancer-Binding Protein-delta
  • Cathepsin K
  • Ctsk protein, mouse