Genetic pleiotropy of ERCC6 loss-of-function and deleterious missense variants links retinal dystrophy, arrhythmia, and immunodeficiency in diverse ancestries

Hum Mutat. 2021 Aug;42(8):969-977. doi: 10.1002/humu.24220. Epub 2021 May 31.

Abstract

Biobanks with exomes linked to electronic health records (EHRs) enable the study of genetic pleiotropy between rare variants and seemingly disparate diseases. We performed robust clinical phenotyping of rare, putatively deleterious variants (loss-of-function [LoF] and deleterious missense variants) in ERCC6, a gene implicated in inherited retinal disease. We analyzed 213,084 exomes, along with a targeted set of retinal, cardiac, and immune phenotypes from two large-scale EHR-linked biobanks. In the primary analysis, a burden of deleterious variants in ERCC6 was strongly associated with (1) retinal disorders; (2) cardiac and electrocardiogram perturbations; and (3) immunodeficiency and decreased immunoglobulin levels. Meta-analysis of results from the BioMe Biobank and UK Biobank showed a significant association of deleterious ERCC6 burden with retinal dystrophy (odds ratio [OR] = 2.6, 95% confidence interval [CI]: 1.5-4.6; p = 8.7 × 10-4 ), atypical atrial flutter (OR = 3.5, 95% CI: 1.9-6.5; p = 6.2 × 10-5 ), arrhythmia (OR = 1.5, 95% CI: 1.2-2.0; p = 2.7 × 10-3 ), and lymphocyte immunodeficiency (OR = 3.8, 95% CI: 2.1-6.8; p = 5.0 × 10-6 ). Carriers of ERCC6 LoF variants who lacked a diagnosis of these conditions exhibited increased symptoms, indicating underdiagnosis. These results reveal a unique genetic link among retinal, cardiac, and immune disorders and underscore the value of EHR-linked biobanks in assessing the full clinical profile of carriers of rare variants.

Keywords: ERCC6; genotype-first diagnosis; pleiotropy; rare variant; whole-exome sequencing.

Publication types

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

MeSH terms

  • Arrhythmias, Cardiac
  • DNA Helicases
  • DNA Repair Enzymes
  • Exome
  • Exome Sequencing / methods
  • Genetic Pleiotropy*
  • Humans
  • Poly-ADP-Ribose Binding Proteins
  • Retinal Dystrophies* / genetics

Substances

  • Poly-ADP-Ribose Binding Proteins
  • DNA Helicases
  • ERCC6 protein, human
  • DNA Repair Enzymes