Local VEGF-A blockade modulates the microenvironment of the corneal graft bed

Am J Transplant. 2019 Sep;19(9):2446-2456. doi: 10.1111/ajt.15331. Epub 2019 Apr 3.

Abstract

The microenvironment plays an important role in several immunological processes. Vascular endothelial growth factor-A (VEGF-A) not only regulates angiogenesis, but is known as a modulator of the immune microenvironment. Modulating the site of transplantation might be beneficial for subsequent transplant survival. In this study, we therefore analyzed the effect that a local blockade of VEGF-A in the inflamed cornea as the graft receiving tissue has on the immune system. We used the murine model of suture-induced neovascularization and subsequent high-risk corneal transplantation, which is an optimal model for local drug application. Mice were treated with VEGFR1/R2 trap prior to transplantation. We analyzed corneal gene expression, as well as protein levels in the cornea and serum on the day of transplantation, 2 and 8 weeks later. Local VEGF depletion prior to transplantation increases the expression of pro-inflammatory as well as immune regulatory cytokines only in the corneal microenvironment, but not in the serum. Furthermore, local VEGFR1/R2 trap treatment significantly inhibits the infiltration of CD11c+ dendritic cells into the cornea. Subsequent increased corneal transplantation success was accompanied by a local upregulation of Foxp3 gene expression. This study demonstrates that locally restricted VEGF depletion increases transplantation success by modulating the receiving corneal microenvironment and inducing tolerogenic mechanisms.

Keywords: basic (laboratory) research/science; chemokines/chemokine receptors; corneal transplantation/ophthalmology; cytokines/cytokine receptors; dendritic cell; immunosuppression/immune modulation; translational research/science; vascular biology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD11 Antigens / metabolism
  • Cornea / blood supply*
  • Cornea / immunology
  • Cornea / pathology
  • Corneal Transplantation*
  • Cytokines / metabolism
  • Dendritic Cells / cytology
  • Disease Models, Animal
  • Female
  • Forkhead Transcription Factors / metabolism
  • Gene Expression Profiling
  • Graft Survival
  • Immune System
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Microcirculation*
  • Neovascularization, Physiologic
  • Sutures
  • Up-Regulation
  • Vascular Endothelial Growth Factor A / antagonists & inhibitors*
  • Vascular Endothelial Growth Factor Receptor-1 / metabolism
  • Vascular Endothelial Growth Factor Receptor-2 / metabolism

Substances

  • CD11 Antigens
  • Cytokines
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Itgax protein, mouse
  • Vascular Endothelial Growth Factor A
  • Kdr protein, mouse
  • Vascular Endothelial Growth Factor Receptor-1
  • Vascular Endothelial Growth Factor Receptor-2