Alterations of retinal vasculature in cystathionine-Beta-synthase mutant mice, a model of hyperhomocysteinemia

Invest Ophthalmol Vis Sci. 2013 Feb 1;54(2):939-49. doi: 10.1167/iovs.12-10536.

Abstract

Purpose: Mice with moderate/severe hyperhomocysteinemia due to deficiency or absence of the cbs gene encoding cystathionine-beta-synthase (CBS) have marked retinal disruption, ganglion cell loss, optic nerve mitochondrial dysfunction, and ERG defects; those with mild hyperhomocysteinemia have delayed retinal morphological/functional phenotype. Excess homocysteine is a risk factor for cardiovascular diseases; however, it is not known whether excess homocysteine alters retinal vasculature.

Methods: Cbs(+/+), cbs(+/-), and cbs(-/-) mice (age ∼3 weeks) were subjected to angiography; retinas were harvested for cryosections, flat-mount preparations, or trypsin digestion and subjected to immunofluorescence microscopy to visualize vessels using isolectin-B4, to detect angiogenesis using anti-VEGF and anti-endoglin (anti-CD105) and activated glial cells (anti-glial fibrillary acidic protein [anti-GFAP]) and to investigate the blood-retinal barrier using the tight junction markers zonula occludens-1 (ZO-1) and occludin. Expression of vegf was determined by quantitative RT-PCR (qRT-PCR) and immunoblotting. Human retinal endothelial cells (HRECs) were treated with excess homocysteine to analyze permeability.

Results: Angiography revealed vascular leakage in cbs(-/-) mice; immunohistochemical analysis demonstrated vascular patterns consistent with ischemia; isolectin-B4 labeling revealed a capillary-free zone centrally and new vessels with capillary tufts midperipherally. This was associated with increased vegf mRNA and protein, CD105, and GFAP in cbs(-/-) retinas concomitant with a marked decrease in ZO-1 and occludin. Homocysteine-treated HRECs showed increased permeability.

Conclusions: Severe elevation of homocysteine in cbs(-/-) mutant mice is accompanied by alterations in retinal vasculature (ischemia, neovascularization, and incompetent blood-retinal barrier). The marked disruption of retinal structure and decreased visual function reported in cbs(-/-) mice may reflect vasculopathy as well as neuropathy.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blood-Retinal Barrier / metabolism
  • Blood-Retinal Barrier / physiopathology
  • Capillary Permeability
  • Cystathionine beta-Synthase / deficiency
  • Cystathionine beta-Synthase / genetics
  • Disease Models, Animal
  • Fluorescein Angiography
  • Fundus Oculi
  • Gene Expression Regulation*
  • Homocysteine / metabolism*
  • Hyperhomocysteinemia / complications
  • Hyperhomocysteinemia / genetics*
  • Hyperhomocysteinemia / metabolism
  • Immunohistochemistry
  • Mice
  • Mice, Mutant Strains
  • Microscopy, Fluorescence
  • RNA, Messenger / genetics*
  • Retina / metabolism
  • Retina / pathology*
  • Retina / physiopathology
  • Retinal Diseases / etiology
  • Retinal Diseases / genetics*
  • Retinal Diseases / pathology
  • Reverse Transcriptase Polymerase Chain Reaction
  • Vascular Endothelial Growth Factor A / biosynthesis
  • Vascular Endothelial Growth Factor A / genetics*

Substances

  • RNA, Messenger
  • Vascular Endothelial Growth Factor A
  • Homocysteine
  • Cystathionine beta-Synthase