Exome-wide Analysis of De Novo and Rare Genetic Variants in Patients With Brain Arteriovenous Malformation

Neurology. 2022 Apr 19;98(16):e1670-e1678. doi: 10.1212/WNL.0000000000200114. Epub 2022 Feb 28.

Abstract

Background and objectives: Brain arteriovenous malformation (bAVM) is a congenital disorder and a leading cause of hemorrhagic stroke. Germline genetic variants play an essential role in the pathogenesis of bAVM. However, the biological relevance of disease-associated genes identified in previous studies is elusive. In this study, we aim to systematically investigate the contribution of germline variants to bAVM and explore the critical molecular pathways underlying the pathogenesis of bAVM.

Methods: Probands with sporadic bAVM were consecutively recruited into this study from November 2015 to November 2018 and underwent exome sequencing. The controls were aggregated from individuals who were not known to have vascular malformation and underwent exome sequencing for clinical or research purposes. The retained control dataset included 4,609 individuals, including 251 individuals with parental samples sequenced. We first analyzed de novo variants in cases and controls and performed a pathway enrichment analysis. A gene-based rare variant association analysis was then performed to identify genes whose variants were significantly enriched in cases.

Results: We collected an exome-sequenced bAVM cohort consisting of 152 trios and 40 singletons. By first focusing on de novo variants, we observed a significant mutational burden of likely gene-disrupting variants in cases vs controls. By performing a pathway enrichment analysis of all nonsynonymous de novo variants identified in cases, we found the angiopoietin-like protein 8 (ANGPTL8) regulatory pathway to be significantly enriched in patients with bAVM. Through an exome-wide rare variant association analysis utilizing 4,394 in-house exome data as controls, we identified SLC19A3 as a disease-associated gene for bAVM. In addition, we found that the SLC19A3 variants in cases are preferably located at the N' side of the SLC19A3 protein. These findings implicate a phenotypic expansion of SLC19A3-related disorders with a domain-specific effect.

Discussion: This study provides insights into the biological basis of bAVM by identifying novel molecular pathways and candidate genes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiopoietin-Like Protein 8
  • Angiopoietin-like Proteins / genetics
  • Brain / pathology
  • Exome / genetics
  • Exome Sequencing
  • Genetic Predisposition to Disease / genetics
  • Humans
  • Intracranial Arteriovenous Malformations* / genetics
  • Intracranial Arteriovenous Malformations* / pathology
  • Membrane Transport Proteins / genetics
  • Mutation
  • Nervous System Malformations*
  • Peptide Hormones* / genetics

Substances

  • ANGPTL8 protein, human
  • Angiopoietin-Like Protein 8
  • Angiopoietin-like Proteins
  • Membrane Transport Proteins
  • Peptide Hormones
  • SLC19A3 protein, human