Mechanosensitive protein polycystin-1 promotes periosteal stem/progenitor cells osteochondral differentiation in fracture healing

Theranostics. 2024 Apr 8;14(6):2544-2559. doi: 10.7150/thno.93269. eCollection 2024.

Abstract

Background: Mechanical forces are indispensable for bone healing, disruption of which is recognized as a contributing cause to nonunion or delayed union. However, the underlying mechanism of mechanical regulation of fracture healing is elusive. Methods: We used the lineage-tracing mouse model, conditional knockout depletion mouse model, hindlimb unloading model and single-cell RNA sequencing to analyze the crucial roles of mechanosensitive protein polycystin-1 (PC1, Pkd1) promotes periosteal stem/progenitor cells (PSPCs) osteochondral differentiation in fracture healing. Results: Our results showed that cathepsin (Ctsk)-positive PSPCs are fracture-responsive and mechanosensitive and can differentiate into osteoblasts and chondrocytes during fracture repair. We found that polycystin-1 declines markedly in PSPCs with mechanical unloading while increasing in response to mechanical stimulus. Mice with conditional depletion of Pkd1 in Ctsk+ PSPCs show impaired osteochondrogenesis, reduced cortical bone formation, delayed fracture healing, and diminished responsiveness to mechanical unloading. Mechanistically, PC1 facilitates nuclear translocation of transcriptional coactivator TAZ via PC1 C-terminal tail cleavage, enhancing osteochondral differentiation potential of PSPCs. Pharmacological intervention of the PC1-TAZ axis and promotion of TAZ nuclear translocation using Zinc01442821 enhances fracture healing and alleviates delayed union or nonunion induced by mechanical unloading. Conclusion: Our study reveals that Ctsk+ PSPCs within the callus can sense mechanical forces through the PC1-TAZ axis, targeting which represents great therapeutic potential for delayed fracture union or nonunion.

Keywords: Fracture healing; Mechanical stress; Periosteal Stem/Progenitor Cells; Polycystin-1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing*
  • Animals
  • Cell Differentiation*
  • Chondrocytes* / metabolism
  • Chondrogenesis / physiology
  • Disease Models, Animal
  • Fracture Healing* / physiology
  • Male
  • Mice
  • Mice, Knockout
  • Osteoblasts / metabolism
  • Osteoblasts / physiology
  • Osteogenesis* / physiology
  • Periosteum / metabolism
  • Stem Cells* / metabolism
  • TRPP Cation Channels* / genetics
  • TRPP Cation Channels* / metabolism

Substances

  • polycystic kidney disease 1 protein
  • TRPP Cation Channels
  • Wwtr1 protein, mouse
  • Adaptor Proteins, Signal Transducing