Superoxide dismutase 2 scavenges ROS to promote osteogenic differentiation of human periodontal ligament stem cells by regulating Smad3 in alveolar bone-defective rats

J Periodontol. 2024 May;95(5):469-482. doi: 10.1002/JPER.23-0469. Epub 2023 Nov 3.

Abstract

Background: Osteogenic differentiation of human periodontal ligament stem cells (hPDLSCs) is an essential event in alveolar bone regeneration. Oxidative stress may be the main inhibiting factor of hPDLSC osteogenesis. Superoxide dismutase 2 (SOD2) is a key antioxidant enzyme, but its effect on hPDLSC osteogenic differentiation is unclear.

Methods: Several surface markers were detected by flow cytometry, and the differentiation potential of hPDLSCs was validated by alkaline phosphatase (ALP), Alizarin Red S, and Oil Red O staining. Osteogenic indicators of hPDLSCs were detected by real-time quantitative polymerase chain reaction (RT-qPCR), Western blotting, and ALP staining. Furthermore, alveolar bone defect rat models were analyzed through micro-CT, hematoxylin and eosin, and Masson staining. The intracellular reactive oxygen species (ROS) level was evaluated by a ROS assay kit. Finally, the expression of SOD2, Smad3, and p-Smad3 in hPDLSCs was detected by RT-qPCR and Western blotting (WB).

Results: SOD2 positively regulated the gene and protein expressions of ALP, BMP6, and RUNX2 in hPDLSCs (p < 0.05). Ideal bone formation and continuous cortical bone were obtained by transplanting LV-SOD2 hPDLSCs (lentivirus vector for overexpressing SOD2 in hPDLSCs) in vivo. Exogenous H2O2 downregulated osteogenic indicators (ALP, BMP6, RUNX2) in hPDLSCs (p < 0.05); this was reversed by overexpression of SOD2. WB results showed that the Smad3 and p-Smad3 signaling pathways participated in the osteogenic process of SOD2 in hPDLSCs.

Conclusion: SOD2 positively regulated hPDLSC osteogenic differentiation in vitro and in vivo. Mechanistically, SOD2 promotes hPDLSC osteogenic differentiation by regulating the phosphorylation of Smad3 to scavenge ROS. This work provides a theoretical basis for the treatment of alveolar bone regeneration.

Keywords: bone regeneration; osteogenesis; reactive oxygen species; superoxide dismutase 2.

MeSH terms

  • Alveolar Bone Loss / metabolism
  • Animals
  • Cell Differentiation*
  • Cells, Cultured
  • Humans
  • Male
  • Osteogenesis* / physiology
  • Periodontal Ligament* / cytology
  • Rats
  • Rats, Sprague-Dawley
  • Reactive Oxygen Species* / metabolism
  • Smad3 Protein* / metabolism
  • Stem Cells*
  • Superoxide Dismutase*

Substances

  • superoxide dismutase 2