Blockade of mTORC1-NOX signaling pathway inhibits TGF-β1-mediated senescence-like structural alterations of the retinal pigment epithelium

FASEB J. 2021 Mar;35(3):e21403. doi: 10.1096/fj.202001939RR.

Abstract

The retinal pigment epithelium (RPE) undergoes characteristic structural changes and epithelial-mesenchymal transition (EMT) during normal aging, which are exacerbated in age-related macular degeneration (AMD). Although the pathogenic mechanisms of aging and AMD remain unclear, transforming growth factor-β1 (TGF-β1) is known to induce oxidative stress, morphometric changes, and EMT as a senescence-promoting factor. In this study, we examined whether intravitreal injection of TGF-β1 into the mouse eye elicits senescence-like morphological alterations in the RPE and if this can be prevented by suppressing mammalian target of rapamycin complex 1 (mTORC1) or NADPH oxidase (NOX) signaling. We verified that intravitreal TGF-β1-induced stress fiber formation and EMT in RPE cells, along with age-associated morphometric changes, including increased variation in cell size and reduced cell density. In RPE cells, exogenous TGF-β1 increased endogenous expression of TGF-β1 and upregulated Smad3-ERK1/2-mTORC1 signaling, increasing reactive oxygen species (ROS) production and EMT. We demonstrated that inhibition of the mTORC1-NOX4 pathway by pretreatment with 5-aminoimidazole-4-carboxamide ribonucleotide (AICAR), an activator of AMP-dependent protein kinase, or GKT137831, a NOX1/4 inhibitor, decreased ROS generation, prevented stress fiber formation, attenuated EMT, and improved the regularity of the RPE structure in vitro and in vivo. These results suggest that intravitreal TGF-β1 injection could be used as a screening model to investigate the aging-related structural and functional changes to the RPE. Furthermore, the regulation of TGF-β-mTORC1-NOX signaling could be a potential therapeutic target for reducing pathogenic alterations in aged RPE and AMD.

Keywords: TGF-β1; epithelial-mesenchymal transition; mTORC1-NOX signaling; retinal pigment epithelium; senescence.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cells, Cultured
  • Cellular Senescence
  • Epithelial-Mesenchymal Transition
  • Intravitreal Injections
  • Macular Degeneration / drug therapy
  • Macular Degeneration / metabolism
  • Male
  • Mechanistic Target of Rapamycin Complex 1 / antagonists & inhibitors
  • Mechanistic Target of Rapamycin Complex 1 / physiology*
  • Mice
  • Mice, Inbred C57BL
  • NADPH Oxidases / antagonists & inhibitors
  • NADPH Oxidases / physiology*
  • Pyrazolones / pharmacology
  • Pyridones / pharmacology
  • Reactive Oxygen Species / metabolism
  • Retinal Pigment Epithelium / pathology*
  • Retinal Pigment Epithelium / physiology
  • Signal Transduction / physiology
  • Transforming Growth Factor beta1 / physiology*

Substances

  • Pyrazolones
  • Pyridones
  • Reactive Oxygen Species
  • Transforming Growth Factor beta1
  • setanaxib
  • NADPH Oxidases
  • Mechanistic Target of Rapamycin Complex 1