ATRX silences Cartpt expression in osteoblastic cells during skeletal development

J Clin Invest. 2025 Jan 2;135(1):e163587. doi: 10.1172/JCI163587.

Abstract

ATP-dependent chromatin remodeling protein ATRX is an essential regulator involved in maintenance of DNA structure and chromatin state and regulation of gene expression during development. ATRX was originally identified as the monogenic cause of X-linked α-thalassemia mental retardation (ATR-X) syndrome. Affected individuals display a variety of developmental abnormalities and skeletal deformities. Studies from others investigated the role of ATRX in skeletal development by tissue-specific Atrx knockout. However, the impact of ATRX during early skeletal development has not been examined. Using preosteoblast-specific Atrx conditional knockout mice, we observed increased trabecular bone mass and decreased osteoclast number in bone. In vitro coculture of Atrx conditional knockout bone marrow stromal cells (BMSCs) with WT splenocytes showed impaired osteoclast differentiation. Additionally, Atrx deletion was associated with decreased receptor activator of nuclear factor κ-B ligand (Rankl)/ osteoprotegerin (Opg) expression ratio in BMSCs. Notably, Atrx-deficient osteolineage cells expressed high levels of the neuropeptide cocaine- and amphetamine-regulated transcript prepropeptide (Cartpt). Mechanistically, ATRX suppresses Cartpt transcription by binding to the promoter, which is otherwise poised for Cartpt expression by RUNX2 binding to the distal enhancer. Finally, Cartpt silencing in Atrx conditional knockout BMSCs rescued the molecular phenotype by increasing the Rankl/Opg expression ratio. Together, our data show a potent repressor function of ATRX in restricting Cartpt expression during skeletal development.

Keywords: Bone biology; Bone development.

MeSH terms

  • Animals
  • Bone Development / genetics
  • Cell Differentiation
  • DNA Helicases* / genetics
  • DNA Helicases* / metabolism
  • Gene Expression Regulation, Developmental
  • Mental Retardation, X-Linked / genetics
  • Mental Retardation, X-Linked / metabolism
  • Mental Retardation, X-Linked / pathology
  • Mesenchymal Stem Cells / cytology
  • Mesenchymal Stem Cells / metabolism
  • Mice
  • Mice, Knockout*
  • Nerve Tissue Proteins* / genetics
  • Nerve Tissue Proteins* / metabolism
  • Nuclear Proteins* / genetics
  • Nuclear Proteins* / metabolism
  • Osteoblasts* / metabolism
  • Osteoclasts / metabolism
  • Osteoprotegerin / genetics
  • Osteoprotegerin / metabolism
  • RANK Ligand* / genetics
  • RANK Ligand* / metabolism
  • X-linked Nuclear Protein* / genetics
  • X-linked Nuclear Protein* / metabolism
  • alpha-Thalassemia / genetics
  • alpha-Thalassemia / metabolism

Substances

  • X-linked Nuclear Protein
  • Atrx protein, mouse
  • Nerve Tissue Proteins
  • Nuclear Proteins
  • DNA Helicases
  • RANK Ligand
  • Tnfsf11 protein, mouse
  • Osteoprotegerin
  • Tnfrsf11b protein, mouse