Effects of vascular endothelial cells on osteogenic differentiation of noncontact co-cultured periodontal ligament stem cells under hypoxia

J Periodontal Res. 2013 Feb;48(1):52-65. doi: 10.1111/j.1600-0765.2012.01503.x. Epub 2012 Aug 21.

Abstract

Background and objective: During periodontitis or orthodontic tooth movement, the periodontal vasculature is severely impaired by chronic inflammation or excessive mechanical force. This leads to a hypoxic microenvironment of the periodontal cells and enhances the expression of various cytokines and growth factors that may regulate angiogenesis and alveolar bone remodeling. However, the role of hypoxia in regulating the communication between endothelial cells (ECs) and osteoblast progenitors during the remodeling and repair of periodontal tissue is still poorly defined. The aim of this study was to investigate the effects of vascular ECs on osteogenic differentiation, mineralization and the paracrine function of noncontact co-cultured periodontal ligament stem cells (PDLSCs) under hypoxia, and further reveal the involvement of MEK/ERK and p38 MAPK pathways in the process.

Material and methods: First, PDLSCs were obtained and a noncontact co-culture system of PDLSCs and human umbilical vein endothelial cells was established. Second, the effects of different time-periods of hypoxia (2% O(2) ) on the osteogenic potential, mineralization and paracrine function of co-cultured PDLSCs were investigated. Third, ERK1/2 and p38 MAPK activities of PDLSCs under hypoxia were measured by western blotting. Finally, we employed specific MAPK inhibitors (PD98059 and SB20350) to investigate the involvement of ERK1/2 and p38 MAPK in PDLSC osteogenesis under hypoxia.

Results: We observed further increased osteogenic differentiation of co-cultured PDLSCs, manifested by markedly enhanced alkaline phosphatase (ALP) activity and prostaglandin E(2) (PGE(2)) levels, vascular endothelial growth factor (VEGF) release, runt-related transcription factor 2 (Runx2) and Sp7 transcriptional and protein levels and mineralized nodule formation, compared with PDLSCs cultured alone. ERK1/2 was phosphorylated in a rapid but transient manner, whereas p38 MAPK was activated in a slow and sustained way under hypoxia. Furthermore, hypoxia-stimulated transcription and expression of osteogenic regulators (hypoxia-inducible factor-1α, ALP, Runx2, Sp7, PGE(2) and VEGF) were also inhibited by PD98059 and SB203580 to different degrees.

Conclusion: Further increased osteogenic differentiation and mineralization of co-cultured PDLSCs under hypoxia were regulated by MEK/ERK and p38 MAPK pathways. And the ECs-mediated paracrine of PGE(2) and VEGF may facilitate the unidirectional PDLSC-EC communication and promote PDLSCs osteogenesis.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Alkaline Phosphatase / analysis
  • Alkaline Phosphatase / drug effects
  • Animals
  • Calcification, Physiologic / physiology
  • Cell Culture Techniques
  • Cell Differentiation / physiology
  • Cell Hypoxia / physiology*
  • Coculture Techniques
  • Core Binding Factor Alpha 1 Subunit / analysis
  • Core Binding Factor Alpha 1 Subunit / drug effects
  • Dinoprostone / analysis
  • Endothelial Cells / physiology*
  • Endothelium, Vascular / cytology*
  • Extracellular Signal-Regulated MAP Kinases / analysis
  • Flavonoids / pharmacology
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / analysis
  • Hypoxia-Inducible Factor 1, alpha Subunit / drug effects
  • Imidazoles / pharmacology
  • MAP Kinase Signaling System / physiology
  • Mice
  • Mitogen-Activated Protein Kinase 1 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 3 / antagonists & inhibitors
  • Osteoblasts / physiology
  • Osteogenesis / physiology*
  • Paracrine Communication / physiology
  • Periodontal Ligament / cytology*
  • Periodontal Ligament / physiology
  • Pyridines / pharmacology
  • Sp7 Transcription Factor
  • Stem Cells / physiology*
  • Transcription Factors / analysis
  • Transcription Factors / drug effects
  • Vascular Endothelial Growth Factor A / analysis
  • Vascular Endothelial Growth Factor A / drug effects
  • p38 Mitogen-Activated Protein Kinases / analysis

Substances

  • Core Binding Factor Alpha 1 Subunit
  • Flavonoids
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Imidazoles
  • Pyridines
  • RUNX2 protein, human
  • Sp7 Transcription Factor
  • SP7 protein, human
  • Transcription Factors
  • VEGFA protein, human
  • Vascular Endothelial Growth Factor A
  • Extracellular Signal-Regulated MAP Kinases
  • MAPK1 protein, human
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • p38 Mitogen-Activated Protein Kinases
  • Alkaline Phosphatase
  • Dinoprostone
  • SB 203580
  • 2-(2-amino-3-methoxyphenyl)-4H-1-benzopyran-4-one