Early degeneration of photoreceptor synapse in Ccl2/Cx3cr1-deficient mice on Crb1(rd8) background

Synapse. 2013 Aug;67(8):515-31. doi: 10.1002/syn.21674. Epub 2013 May 27.

Abstract

Photoreceptor ribbon synapse releases glutamate to postsynaptic targets. The synaptic ribbon may play multiple roles in ribbon synapse development, synaptic vesicle recycling, and synaptic transmission. Age-related macular degeneration (AMD) patients appear to have fewer or no detectable synaptic ribbons as well as abnormal swelling in the photoreceptor terminals in the macula. However, reports on changes of photoreceptor synapses in AMD are scarce and photoreceptor type and quantity affected in early AMD is still unclear. Here, we employed multiple anatomical techniques to investigate these questions in Ccl2⁻/⁻/Cx3cr1⁻/⁻ mouse on Crb1(rd8) background (DKO rd8) at one month of age. We found that approximately 17% of photoreceptors over the focal lesion were lost. Immunostaining for synapse-associated proteins (CtBP2, synaptophysin, and vesicular glutamate transporter 1) showed significantly reduced expression and ectopic localization. Cone opsins demonstrated dramatic reduction in expression (S-opsins) and extensive mislocalization (M-opsins). Quantitative ultrastructural analysis confirmed a significant decrease in the number of cone terminals and nuclei, numerous vacuoles in remaining cone terminals, reduction in the number of synaptic ribbons in photoreceptor terminals, and ectopic rod ribbon synapses. In addition, glutamate receptor immunoreactivity on aberrant sprouting of rod bipolar cells and horizontal cells were identified at the ectopic synapses. These results indicate that synaptic alterations occur at the early stages of disease and cones are likely more susceptible to damage caused by DKO rd8 mutation. They provide a new insight into potential mechanism of vision function lost due to synaptic degeneration before cell death in the early stages of AMD.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Alcohol Oxidoreductases
  • Animals
  • CX3C Chemokine Receptor 1
  • Cell Nucleus / ultrastructure
  • Chemokine CCL2 / genetics*
  • Chemokine CCL2 / metabolism
  • Co-Repressor Proteins
  • Cone Opsins / genetics
  • Cone Opsins / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Macula Lutea / abnormalities
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mutation
  • Nerve Tissue Proteins / genetics*
  • Nerve Tissue Proteins / metabolism
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism
  • Photoreceptor Cells, Vertebrate / metabolism*
  • Photoreceptor Cells, Vertebrate / pathology
  • Receptors, Chemokine / genetics*
  • Receptors, Chemokine / metabolism
  • Synapses / genetics
  • Synapses / ultrastructure*
  • Synaptic Vesicles / ultrastructure
  • Synaptophysin / genetics
  • Synaptophysin / metabolism
  • Vesicular Monoamine Transport Proteins / genetics
  • Vesicular Monoamine Transport Proteins / metabolism

Substances

  • CX3C Chemokine Receptor 1
  • Ccl2 protein, mouse
  • Chemokine CCL2
  • Co-Repressor Proteins
  • Cone Opsins
  • Crb1 protein, mouse
  • Cx3cr1 protein, mouse
  • DNA-Binding Proteins
  • Nerve Tissue Proteins
  • Phosphoproteins
  • Receptors, Chemokine
  • Slc18a1 protein, mouse
  • Synaptophysin
  • Vesicular Monoamine Transport Proteins
  • Alcohol Oxidoreductases
  • Ctbp2 protein, mouse