Role of the Norrie disease pseudoglioma gene in sprouting angiogenesis during development of the retinal vasculature

Invest Ophthalmol Vis Sci. 2005 Sep;46(9):3372-82. doi: 10.1167/iovs.05-0174.

Abstract

Purpose: To characterize developmental defects and the time course of Norrie disease in retinal and hyaloid vasculature during retinal development and to identify underlying molecular angiogenic pathways that may be affected in Norrie disease, exudative vitreoretinopathy, retinopathy of prematurity, and Coats' disease.

Methods: Norrie disease pseudoglioma homologue (Ndph)-knockout mice were studied during retinal development at early postnatal (p) stages (p5, p10, p15, and p21). Histologic techniques, quantitative RT-PCR, ELISA, and Western blot analyses provided molecular data, and scanning laser ophthalmoscopy (SLO) angiography and electroretinography (ERG) were used to obtain in vivo data.

Results: The data showed that regression of the hyaloid vasculature of Ndph-knockout mice occurred but was drastically delayed. The development of the superficial retinal vasculature was strongly delayed, whereas the deep retinal vasculature did not form because of the blockage of vessel outgrowth into the deep retinal layers. Subsequently, microaneurysm-like lesions formed. Several angiogenic factors were differentially transcribed during retinal development. Increased levels of hypoxia inducible factor-1alpha (HIF1alpha) and VEGFA, as well as a characteristic ERG pattern, confirmed hypoxic conditions in the inner retina of the Ndph-knockout mouse.

Conclusions: These data provide evidence for a crucial role of Norrin in hyaloid vessel regression and in sprouting angiogenesis during retinal vascular development, especially in the development of the deep retinal capillary networks. They also suggest an early and a late phase of Norrie disease and may provide an explanation for similar phenotypic features of allelic retinal diseases in mice and patients as secondary consequences of pathologic hypoxia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blotting, Western
  • DNA-Binding Proteins / metabolism
  • Electroretinography
  • Enzyme-Linked Immunosorbent Assay
  • Eye Proteins / physiology*
  • Fluorescein Angiography
  • Gene Expression / physiology
  • Humans
  • Hypoxia / metabolism
  • Hypoxia-Inducible Factor 1
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Infant, Newborn
  • Mice
  • Mice, Knockout
  • Nerve Tissue Proteins / physiology*
  • Nuclear Proteins / metabolism
  • Ophthalmic Artery / physiopathology*
  • Ophthalmoscopy
  • Retinal Neovascularization / metabolism*
  • Retinal Neovascularization / pathology
  • Retinal Vessels / growth & development*
  • Retinal Vessels / pathology
  • Retinopathy of Prematurity / metabolism*
  • Retinopathy of Prematurity / pathology
  • Reverse Transcriptase Polymerase Chain Reaction
  • Transcription Factors / metabolism
  • Vascular Endothelial Growth Factor A / metabolism
  • Vitreoretinopathy, Proliferative / metabolism*
  • Vitreoretinopathy, Proliferative / pathology
  • Vitreous Body / blood supply*

Substances

  • DNA-Binding Proteins
  • Eye Proteins
  • HIF1A protein, human
  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Ndph protein, mouse
  • Nerve Tissue Proteins
  • Nuclear Proteins
  • Transcription Factors
  • Vascular Endothelial Growth Factor A
  • vascular endothelial growth factor A, mouse