Cone dystrophy and ectopic synaptogenesis in a Cacna1f loss of function model of congenital stationary night blindness (CSNB2A)

Channels (Austin). 2018 Jan 1;12(1):17-33. doi: 10.1080/19336950.2017.1401688. Epub 2018 Jan 2.

Abstract

Congenital stationary night blindness 2A (CSNB2A) is an X-linked retinal disorder, characterized by phenotypically variable signs and symptoms of impaired vision. CSNB2A is due to mutations in CACNA1F, which codes for the pore-forming α1F subunit of a L-type voltage-gated calcium channel, Cav1.4. Mouse models of CSNB2A, used for characterizing the effects of various Cacna1f mutations, have revealed greater severity of defects than in human CSNB2A. Specifically, Cacna1f-knockout mice show an apparent lack of visual function, gradual retinal degeneration, and disruption of photoreceptor synaptic terminals. Several reports have also noted cone-specific disruptions, including axonal abnormalities, dystrophy, and cell death. We have explored further the involvement of cones in our 'G305X' mouse model of CSNB2A, which has a premature truncation, loss-of-function mutation in Cacna1f. We show that the expression of genes for several phototransduction-related cone markers is down-regulated, while that of several cellular stress- and damage-related markers is up-regulated; and that cone photoreceptor structure and photopic visual function - measured by immunohistochemistry, optokinetic response and electroretinography - deteriorate progressively with age. We also find that dystrophic cone axons establish synapse-like contacts with rod bipolar cell dendrites, which they normally do not contact in wild-type retinas - ectopically, among rod cell bodies in the outer nuclear layer. These data support a role for Cav1.4 in cone synaptic development, cell viability, and synaptic transmission of cone-dependent visual signals. Although our novel finding of cone-to-rod-bipolar cell contacts in this mouse model of a retinal channelopathy may challenge current views of the role of Cav1.4 in photopic vision, it also suggests a potential new target for restorative therapy.

Keywords: CSNB; Cacna1f; Cav1.4; channelopathy; photoreceptor; retina.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium Channels / deficiency
  • Calcium Channels / genetics
  • Calcium Channels / metabolism*
  • Calcium Channels, L-Type
  • Cone Dystrophy / metabolism*
  • Disease Models, Animal*
  • Eye Diseases, Hereditary / metabolism*
  • Eye Diseases, Hereditary / pathology
  • Female
  • Genetic Diseases, X-Linked / metabolism*
  • Genetic Diseases, X-Linked / pathology
  • Mice
  • Mice, Knockout
  • Mutation
  • Myopia / metabolism*
  • Myopia / pathology
  • Night Blindness / metabolism*
  • Night Blindness / pathology
  • Synapses / metabolism*

Substances

  • Cacna1f protein, mouse
  • Calcium Channels
  • Calcium Channels, L-Type

Supplementary concepts

  • Night blindness, congenital stationary

Grants and funding