Prorenin receptor (PRR)-mediated NADPH oxidase (Nox) signaling regulates VEGF synthesis under hyperglycemic condition in ARPE-19 cells

J Recept Signal Transduct Res. 2017 Dec;37(6):560-568. doi: 10.1080/10799893.2017.1369120. Epub 2017 Aug 25.

Abstract

The stimulation of angiotensin II (Ang II), the effector peptide of renin-angiotensin system, has been reported to increase the expression of vascular endothelial growth factor (VEGF) through the activation of the Ang II type 1 receptor (AT1R). In this study, we investigated whether hyperglycemia (HG, 33 mM glucose) in ARPE-19 cells could promote the expression of VEGF independently of Ang II through prorenin receptor (PRR), via an NADPH oxidase (Nox)-dependent mechanism. ARPE-19 cells were treated with the angiotensin converting enzyme (ACE) inhibitor perindopril to block the synthesis of Ang II. Treatment with HG induced VEGF expression in ARPE-19 cells, which was attenuated by pretreatment with the inhibitors of Nox, but not those of nitric oxide synthase, xanthine oxidase and mitochondrial O2 synthesis. In addition, Nox-derived [Formula: see text] and H2O2 signaling in the regulation of VEGF was determined by using both polyethylene glycol (PEG)-catalase (CAT) and PEG-superoxide dismutase (SOD). We demonstrated that small interfering RNA (siRNA)-mediated knockdown of PRR, Nox2 and Nox4 significantly reduced the HG-induced stimulation of VEGF. On the other hand, Nox4 overexpression significantly potentiated PRR-induced stimulation of VEGF under hyperglycemia in ARPE-19 cells. Furthermore, Nox4 was shown to be associated with enhanced activities of ERK1/2 and NF-κB (p65), indicating their involvement in PRR-induced activation of VEGF under HG in ARPE-19 cells. Our results support the hypothesis that Nox4-derived reactive oxygen species (ROS) signaling is implicated in the hyperglycemia-induced increase of VEGF expression through PRR in ARPE-19 cells. However, further work is needed to evaluate the role of PRR and Nox-s in HG-induced stimulation of VEGF in vivo.

Keywords: NADPH oxidase (Nox); Prorenin receptor; VEGF; diabetic retinopathy; renin–angiotensin system (RAS); retina.

MeSH terms

  • Gene Expression Regulation / genetics
  • Humans
  • Hyperglycemia / chemically induced
  • Hyperglycemia / genetics*
  • Hyperglycemia / pathology
  • Mitochondria / genetics
  • Mitochondria / metabolism
  • NADPH Oxidase 2 / antagonists & inhibitors
  • NADPH Oxidase 2 / genetics*
  • NADPH Oxidase 4 / antagonists & inhibitors
  • NADPH Oxidase 4 / genetics*
  • Oxidation-Reduction
  • Oxidative Stress / genetics
  • Prorenin Receptor
  • RNA, Small Interfering / genetics
  • Reactive Oxygen Species / metabolism
  • Receptor, Angiotensin, Type 1 / genetics
  • Receptors, Cell Surface / antagonists & inhibitors
  • Receptors, Cell Surface / genetics*
  • Renin / genetics
  • Renin-Angiotensin System / genetics
  • Signal Transduction / drug effects
  • Vascular Endothelial Growth Factor A / genetics*

Substances

  • RNA, Small Interfering
  • Reactive Oxygen Species
  • Receptor, Angiotensin, Type 1
  • Receptors, Cell Surface
  • Vascular Endothelial Growth Factor A
  • CYBB protein, human
  • NADPH Oxidase 2
  • NADPH Oxidase 4
  • NOX4 protein, human
  • Renin
  • Prorenin Receptor