Semaphorin 4D Enhances Angiogenic Potential and Suppresses Osteo-/Odontogenic Differentiation of Human Dental Pulp Stem Cells

J Endod. 2017 Feb;43(2):297-305. doi: 10.1016/j.joen.2016.10.019. Epub 2016 Dec 24.

Abstract

Introduction: To investigate the roles of semaphorin 4D (Sema4D)/plexin-B1 signaling on the angiogenic potential and osteo-/odontogenic differentiation of human dental pulp stem cells (DPSCs) and to uncover the corresponding molecular mechanisms.

Methods: DPSCs were treated with Sema4D (10 μg/mL) for different time durations. Osteo-/odontogenic differentiation was assessed by quantifying alkaline phosphatase activity, mineralized nodule formation, and osteo-/odontogenic gene (ALP, Col1A1, BSP, RUNX2, and DSPP) and protein (Col1A1 and DSPP) expression. Involvement of the Sema4D/plexin-B1 signaling pathway was analyzed by Western blot analysis. Additionally, angiogenic gene and protein expression was assessed by reverse-transcription polymerase chain reaction and enzyme-linked immunosorbent assay. In vitro endothelial tube formation assay on Matrigel (BD Biosciences, San Jose, CA) was performed to evaluate the angiogenic inductive potential of the Sema4D-treated DPSCs conditioned medium. Results were analyzed using 1-way analysis of variance and the Student t test.

Results: Sema4D significantly inhibited ALP activity and mineralized nodule formation of DPSCs. Furthermore, Sema4D-treated DPSCs displayed marked down-regulation in the expression of osteo-/odontogenic genes (ALP, Col1A1, BSP, RUNX2, and DSPP) as well as proteins (Col1A1 and DSPP). Elevated levels of plexin-B1 and downstream RhoA protein expression together with phosphorylated plexin-B1 confirmed the involvement of Sema4D/plexin-B1 signaling. Protein expression of ErbB2 was up-regulated, and Met was slightly down-regulated. Furthermore, Sema4D-treated DPSCs exhibited enhanced expression of vascular endothelial growth factor at both the messenger RNA and protein level. Accordingly, the conditioned medium of Sema4D-treated DPSCs promoted the formation of vessel-like structures as shown by the Matrigel assay.

Conclusions: Sema4D markedly enhances the angiogenic potential but suppresses osteo-/odontogenic differentiation of DPSCs. Sema4D/plexin-B signaling was activated via the RhoA-mediated pathway.

Keywords: Alkaline phosphatase activity; angiogenic potential; dental pulp stem cells; osteo-/odontogenic differentiation; semaphorin 4D/plexin-B1.

MeSH terms

  • Alkaline Phosphatase / metabolism
  • Antigens, CD / pharmacology*
  • Blotting, Western
  • Cell Differentiation / drug effects
  • Cell Proliferation / drug effects
  • Cells, Cultured
  • Dental Pulp / cytology
  • Dental Pulp / drug effects*
  • Dental Pulp / growth & development
  • Enzyme-Linked Immunosorbent Assay
  • Humans
  • Neovascularization, Physiologic / drug effects
  • Real-Time Polymerase Chain Reaction
  • Semaphorins / pharmacology*
  • Stem Cells / drug effects*
  • Stem Cells / physiology
  • Vascular Endothelial Growth Factor A / metabolism

Substances

  • Antigens, CD
  • CD100 antigen
  • Semaphorins
  • Vascular Endothelial Growth Factor A
  • Alkaline Phosphatase