Doxycycline inhibits inflammation-induced lymphangiogenesis in mouse cornea by multiple mechanisms

PLoS One. 2014 Sep 30;9(9):e108931. doi: 10.1371/journal.pone.0108931. eCollection 2014.

Abstract

Lymphangiogenesis is significantly involved in the pathogenesis of diseases, including graft rejection, cancer metastasis and various inflammatory conditions. The inhibition of lymphangiogenesis has become a new therapeutic target for the treatment of these diseases. Here, we explored the anti-lymphangiogenic effects of doxycycline in inflammation-induced lymphangiogenesis (ILA) in the cornea and the underlying mechanisms. In the present study, mice with ILA of the cornea were treated with topical doxycycline (0.1%) or vehicle control. Lymphangiogenesis was quantified using corneal immunostaining of lymphatic vessel endothelial hyaluronan receptor-1 (LYVE-1). Human dermal lymphatic endothelial cells (HDLECs) and a murine macrophage cell line (RAW264.7) were used to further explore the underlying mechanisms of doxycycline-mediated anti-lymphangiogenesis in vitro. Our results showed that doxycycline treatment dramatically inhibited ILA in the mouse cornea (p<0.001), with a significant decrease in vascular endothelial growth factor (VEGF)-C/VEGF receptor 3 signalling, macrophage infiltration and inflammatory cytokine expression. Doxycycline also significantly inhibited VEGF-C-induced HDLEC proliferation in vitro by modulating the PI3K/Akt/endothelial nitric oxide (NO) synthase (eNOS) pathway and significantly suppressed interleukin-1β (IL-1β), TNF-α and VEGF-C production in the RAW264.7 cell line by modulating the PI3K/Akt/nuclear factor-kappaB (NF-κB) pathway. Additionally, doxycycline treatment dramatically reduced the phosphorylation of NF-κBp65, Akt and eNOS in ILA and significantly inhibited matrix metalloproteinases (MMPs) activity in vitro and in ILA. In conclusion, doxycycline inhibited ILA, possibly through suppression of VEGF-C signalling, macrophage function and MMPs activity. This observation suggests that doxycycline is a potential therapeutic agent for lymphangiogenesis-related diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Cell Proliferation / drug effects
  • Cornea / drug effects*
  • Cornea / metabolism
  • Doxycycline / pharmacology*
  • Female
  • Glycoproteins / immunology
  • Glycoproteins / metabolism
  • Humans
  • Hydrogel, Polyethylene Glycol Dimethacrylate / chemistry
  • Inflammation / pathology
  • Lipopolysaccharides / toxicity
  • Lymphangiogenesis / drug effects*
  • Lymphocyte Activation / drug effects
  • Membrane Transport Proteins
  • Mice
  • Mice, Inbred C57BL
  • Nitric Oxide / metabolism
  • Nitric Oxide Synthase Type III / metabolism
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphorylation / drug effects
  • Proto-Oncogene Proteins c-akt / metabolism
  • Signal Transduction / drug effects
  • Vascular Endothelial Growth Factor C / metabolism
  • Vascular Endothelial Growth Factor C / pharmacology
  • Vascular Endothelial Growth Factor Receptor-3 / metabolism

Substances

  • Glycoproteins
  • Lipopolysaccharides
  • Membrane Transport Proteins
  • Vascular Endothelial Growth Factor C
  • Xlkd1 protein, mouse
  • Hydrogel, Polyethylene Glycol Dimethacrylate
  • Nitric Oxide
  • Nitric Oxide Synthase Type III
  • Vascular Endothelial Growth Factor Receptor-3
  • Proto-Oncogene Proteins c-akt
  • Doxycycline

Grants and funding

This work was supported by the Natural Science Foundation of China: 81271051 and 81300740. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.