Canonical ligand-dependent and non-canonical ligand-independent EphA2 signaling in the eye lens of wild-type, knockout, and aging mice

Aging (Albany NY). 2024 Oct 25;16(20):13039-13075. doi: 10.18632/aging.206144. Epub 2024 Oct 25.

Abstract

Disruption of Eph-ephrin bidirectional signaling leads to human congenital and age-related cataracts, but the mechanisms for these opacities in the eye lens remain unclear. Eph receptors bind to ephrin ligands on neighboring cells to induce canonical ligand-mediated signaling. The EphA2 receptor also signals non-canonically without ligand binding in cancerous cells, leading to epithelial-to-mesenchymal transition (EMT). We have previously shown that the receptor EphA2 and the ligand ephrin-A5 have diverse functions in maintaining lens transparency in mice. Loss of ephrin-A5 leads to anterior cataracts due to EMT. Surprisingly, both canonical and non-canonical EphA2 activation are present in normal wild-type lenses and in the ephrin-A5 knockout lenses. Canonical EphA2 signaling is localized exclusively to lens epithelial cells and does not change with age. Non-canonical EphA2 signaling is in both epithelial and fiber cells and increases significantly with age. We hypothesize that canonical ligand-dependent EphA2 signaling is required for the morphogenesis and organization of hexagonal equatorial epithelial cells while non-canonical ligand-independent EphA2 signaling is needed for complex membrane interdigitations that change during fiber cell differentiation and maturation. This is the first demonstration of non-canonical EphA2 activation in a non-cancerous tissue or cell and suggests a possible physiological function for ligand-independent EphA2 signaling.

Keywords: S897; Y588; Y589; ephrin; epithelial cells; fiber cells; maturation; phosphorylation.

MeSH terms

  • Aging* / genetics
  • Aging* / metabolism
  • Animals
  • Cataract / genetics
  • Cataract / metabolism
  • Cataract / pathology
  • Ephrin-A5 / genetics
  • Ephrin-A5 / metabolism
  • Epithelial Cells / metabolism
  • Epithelial-Mesenchymal Transition / genetics
  • Lens, Crystalline* / metabolism
  • Ligands
  • Mice
  • Mice, Knockout*
  • Receptor, EphA2* / genetics
  • Receptor, EphA2* / metabolism
  • Signal Transduction*

Substances

  • Receptor, EphA2
  • Ligands
  • Ephrin-A5