Putative digenic inheritance of heterozygous RP1L1 and C2orf71 null mutations in syndromic retinal dystrophy

Ophthalmic Genet. 2017 Mar-Apr;38(2):127-132. doi: 10.3109/13816810.2016.1151898. Epub 2016 Mar 30.

Abstract

Background: Retinitis pigmentosa (RP) is the most common cause of inherited retinal degeneration and can occur in non-syndromic and syndromic forms. Syndromic RP is accompanied by other symptoms such as intellectual disability, hearing loss, or congenital abnormalities. Both forms are known to exhibit complex genetic interactions that can modulate the penetrance and expressivity of the phenotype.

Materials and methods: In an individual with atypical RP, hearing loss, ataxia and cerebellar atrophy, whole exome sequencing was performed. The candidate pathogenic variants were tested by developing an in vivo zebrafish model and assaying for retinal and cerebellar integrity.

Results: Exome sequencing revealed a complex heterozygous protein-truncating mutation in RP1L1, p.[(Lys111Glnfs*27; Gln2373*)], and a heterozygous nonsense mutation in C2orf71, p.(Ser512*). Mutations in both genes have previously been implicated in autosomal recessive non-syndromic RP, raising the possibility of a digenic model in this family. Functional testing in a zebrafish model for two key phenotypes of the affected person showed that the combinatorial suppression of rp1l1 and c2orf71l induced discrete pathology in terms of reduction of eye size with concomitant loss of rhodopsin in the photoreceptors, and disorganization of the cerebellum.

Conclusions: We propose that the combination of heterozygous loss-of-function mutations in these genes drives syndromic retinal dystrophy, likely through the genetic interaction of at least two loci. Haploinsufficiency at each of these loci is insufficient to induce overt pathology.

Keywords: Cerebellum; ciliopathy; digenic inheritance; hearing loss; retinitis pigmentosa; zebrafish.

MeSH terms

  • Adult
  • Animals
  • Comparative Genomic Hybridization
  • DNA Mutational Analysis
  • Disease Models, Animal
  • Embryo, Nonmammalian
  • Exome / genetics
  • Eye Proteins / genetics*
  • Female
  • Gene Silencing
  • Genetic Predisposition to Disease*
  • Heterozygote
  • Humans
  • Inheritance Patterns*
  • Mutation / genetics*
  • Pedigree
  • Retinitis Pigmentosa / genetics*
  • Retinitis Pigmentosa / pathology
  • Rhodopsin / genetics
  • Sequence Analysis, DNA
  • Zebrafish / embryology
  • Zebrafish Proteins / genetics

Substances

  • Eye Proteins
  • PCARE protein, human
  • RP1L1 protein, human
  • Zebrafish Proteins
  • Rhodopsin