Diminished Canonical β-Catenin Signaling During Osteoblast Differentiation Contributes to Osteopenia in Progeria

J Bone Miner Res. 2018 Nov;33(11):2059-2070. doi: 10.1002/jbmr.3549. Epub 2018 Aug 1.

Abstract

Patients with Hutchinson-Gilford progeria syndrome (HGPS) have low bone mass and an atypical skeletal geometry that manifests in a high risk of fractures. Using both in vitro and in vivo models of HGPS, we demonstrate that defects in the canonical WNT/β-catenin pathway, seemingly at the level of the efficiency of nuclear import of β-catenin, impair osteoblast differentiation and that restoring β-catenin activity rescues osteoblast differentiation and significantly improves bone mass. Specifically, we show that HGPS patient-derived iPSCs display defects in osteoblast differentiation, characterized by a decreased alkaline phosphatase activity and mineralizing capacity. We demonstrate that the canonical WNT/β-catenin pathway, a major signaling cascade involved in skeletal homeostasis, is impaired by progerin, causing a reduction in the active β-catenin in the nucleus and thus decreased transcriptional activity, and its reciprocal cytoplasmic accumulation. Blocking farnesylation of progerin restores active β-catenin accumulation in the nucleus, increasing signaling, and ameliorates the defective osteogenesis. Moreover, in vivo analysis of the Zmpste24-/- HGPS mouse model demonstrates that treatment with a sclerostin-neutralizing antibody (SclAb), which targets an antagonist of canonical WNT/β-catenin signaling pathway, fully rescues the low bone mass phenotype to wild-type levels. Together, this study reveals that the β-catenin signaling cascade is a therapeutic target for restoring defective skeletal microarchitecture in HGPS. © 2018 American Society for Bone and Mineral Research.

Keywords: HGPS; MESENCHYMAL STEM CELL; OSTEOGENIC DIFFERENTIATION AND AGING; PROGERIA; WNT/β-CATENIN SIGNALING.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Animals
  • Antibodies, Neutralizing / pharmacology
  • Bone Diseases, Metabolic / complications*
  • Bone Diseases, Metabolic / metabolism*
  • Bone Diseases, Metabolic / pathology
  • Cell Differentiation* / drug effects
  • Cell Line
  • Disease Models, Animal
  • Glycoproteins / immunology
  • Humans
  • Induced Pluripotent Stem Cells / metabolism
  • Intercellular Signaling Peptides and Proteins
  • Lamin Type A / metabolism
  • Mesenchymal Stem Cells / drug effects
  • Mesenchymal Stem Cells / metabolism
  • Mice
  • Models, Biological
  • Mutation / genetics
  • Osteoblasts / drug effects
  • Osteoblasts / metabolism*
  • Osteogenesis / drug effects
  • Phenotype
  • Progeria / complications*
  • Progeria / genetics
  • Progeria / metabolism*
  • Progeria / pathology
  • Protein Prenylation / drug effects
  • Signal Transduction*
  • Wnt Signaling Pathway / drug effects
  • beta Catenin / metabolism*

Substances

  • Adaptor Proteins, Signal Transducing
  • Antibodies, Neutralizing
  • Glycoproteins
  • Intercellular Signaling Peptides and Proteins
  • Lamin Type A
  • Sost protein, mouse
  • beta Catenin
  • prelamin A