ARPE-19-derived VEGF-containing exosomes promote neovascularization in HUVEC: the role of the melanocortin receptor 5

Cell Cycle. 2019 Feb;18(4):413-424. doi: 10.1080/15384101.2019.1568745. Epub 2019 Feb 9.

Abstract

ARPE-19 retinal pigment epithelial cells cultured in a medium containing 35 mM D-glucose led to an augmented ROS formation and release of vascular endothelial factor (VEGF)-containing exosomes compared to ARPE-19 cells cultured in a medium containing 5 mM D-glucose (standard medium). Exposing these cells to the melanocortin 5 receptor agonist (MCR5) PG-901 (10-10M), for 9 d reduced ROS generation, the number of exosomes released and their VEGF content. In contrast, incubating the cells with the melanocortin receptor MCR1 agonist BMS-470539 (10-5 M) or with the mixed MCR3/4 agonist MTII (0.30 nmol) did not produce any significant decrease in ROS levels. ARPE-19-derived VEGF-containing exosomes promoted neovascularization in human umbilical vein endothelial cells (HUVEC), an effect that was markedly reduced by PG-901 (10-10M) but not by the MCR3/4 agonist MTII (0.30 nmol) or the MCR1 agonist BMS-470539 (10-5 M). The MCR5-related action in the ARPE-19 cells was accompanied by the increased expression of two coupled factors, cytochrome p4502E1 (CYP2E1) and nuclear factor kappa b (Nf-κB). These are both involved in high glucose signalling, in ROS generation and, interestingly, were reduced by the MCR5 agonist in the ARPE-19 cells. Altogether, these data suggest that MCR5 is a modulator of the responses stimulated by glucose in ARPE-19 cells, which might possibly be translated into a modulation of the retinal pigment epithelium response to diabetes in vivo.

Keywords: Diabetes; exosomes; melanocortin receptors; oxidative stress; vasculogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line
  • Cell Survival / drug effects
  • Culture Media / chemistry
  • Cytochrome P-450 CYP2E1 / metabolism
  • Exosomes / metabolism*
  • Glucose / metabolism
  • Human Umbilical Vein Endothelial Cells / metabolism*
  • Humans
  • Imidazoles / pharmacology
  • NF-kappa B / metabolism
  • Neovascularization, Physiologic / drug effects
  • Neovascularization, Physiologic / physiology*
  • Peptides, Cyclic / pharmacology
  • Reactive Oxygen Species / metabolism
  • Receptor, Melanocortin, Type 1 / agonists
  • Receptor, Melanocortin, Type 3 / agonists
  • Receptors, Melanocortin / agonists
  • Receptors, Melanocortin / metabolism*
  • Retinal Pigment Epithelium / metabolism*
  • Signal Transduction / drug effects
  • Vascular Endothelial Growth Factor A / metabolism*
  • alpha-MSH / analogs & derivatives
  • alpha-MSH / pharmacology

Substances

  • BMS-470539
  • Culture Media
  • Imidazoles
  • MC1R protein, human
  • MC3R protein, human
  • NF-kappa B
  • PG 901
  • Peptides, Cyclic
  • Reactive Oxygen Species
  • Receptor, Melanocortin, Type 1
  • Receptor, Melanocortin, Type 3
  • Receptors, Melanocortin
  • VEGFA protein, human
  • Vascular Endothelial Growth Factor A
  • acetyl-norleucyl(4)-(aspartyl(5)-histidyl(6)-phenylalanyl(7)-arginyl(8)-tryptophyl(9)-lysyl(10))cyclo-alpha-MSH(4-10)amide
  • melanocortin 5 receptor
  • alpha-MSH
  • Cytochrome P-450 CYP2E1
  • Glucose

Grants and funding

This work was partially supported by grant PROMETEO #94/2016 from Generalitat Valenciana, Valencia, Spain.