SSBP1 mutations in dominant optic atrophy with variable retinal degeneration

Ann Neurol. 2019 Sep;86(3):368-383. doi: 10.1002/ana.25550. Epub 2019 Jul 31.

Abstract

Objective: Autosomal dominant optic atrophy (ADOA) starts in early childhood with loss of visual acuity and color vision deficits. OPA1 mutations are responsible for the majority of cases, but in a portion of patients with a clinical diagnosis of ADOA, the cause remains unknown. This study aimed to identify novel ADOA-associated genes and explore their causality.

Methods: Linkage analysis and sequencing were performed in multigeneration families and unrelated patients to identify disease-causing variants. Functional consequences were investigated in silico and confirmed experimentally using the zebrafish model.

Results: We defined a new ADOA locus on 7q33-q35 and identified 3 different missense variants in SSBP1 (NM_001256510.1; c.113G>A [p.(Arg38Gln)], c.320G>A [p.(Arg107Gln)] and c.422G>A [p.(Ser141Asn)]) in affected individuals from 2 families and 2 singletons with ADOA and variable retinal degeneration. The mutated arginine residues are part of a basic patch that is essential for single-strand DNA binding. The loss of a positive charge at these positions is very likely to lower the affinity of SSBP1 for single-strand DNA. Antisense-mediated knockdown of endogenous ssbp1 messenger RNA (mRNA) in zebrafish resulted in compromised differentiation of retinal ganglion cells. A similar effect was achieved when mutated mRNAs were administered. These findings point toward an essential role of ssbp1 in retinal development and the dominant-negative nature of the identified human variants, which is consistent with the segregation pattern observed in 2 multigeneration families studied.

Interpretation: SSBP1 is an essential protein for mitochondrial DNA replication and maintenance. Our data have established pathogenic variants in SSBP1 as a cause of ADOA and variable retinal degeneration. ANN NEUROL 2019;86:368-383.

Publication types

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

MeSH terms

  • Animals
  • Cell Differentiation / genetics
  • Cells, Cultured
  • DNA-Binding Proteins / genetics*
  • Female
  • Gene Knockdown Techniques
  • Genetic Linkage / genetics
  • Genetic Predisposition to Disease / genetics*
  • Humans
  • Male
  • Mice
  • Mitochondrial Proteins / genetics*
  • Mutation, Missense
  • Optic Atrophy, Autosomal Dominant / genetics*
  • Optic Atrophy, Autosomal Dominant / pathology
  • Pedigree
  • RNA, Messenger / genetics
  • Retinal Degeneration / genetics
  • Retinal Degeneration / pathology
  • Zebrafish / genetics

Substances

  • DNA-Binding Proteins
  • Mitochondrial Proteins
  • RNA, Messenger
  • SSBP1 protein, human