Truncating variant burden in high-functioning autism and pleiotropic effects of LRP1 across psychiatric phenotypes

J Psychiatry Neurosci. 2019 Sep 1;44(5):350-359. doi: 10.1503/jpn.180184.

Abstract

Background: Previous research has implicated de novo and inherited truncating mutations in autism-spectrum disorder. We aim to investigate whether the load of inherited truncating mutations contributes similarly to high-functioning autism, and to characterize genes that harbour de novo variants in high-functioning autism.

Methods: We performed whole-exome sequencing in 20 high-functioning autism families (average IQ = 100).

Results: We observed no difference in the number of transmitted versus nontransmitted truncating alleles for high-functioning autism (117 v. 130, p = 0.78). Transmitted truncating and de novo variants in high-functioning autism were not enriched in gene ontology (GO) or Kyoto Encyclopedia of Genes and Genomes (KEGG) categories, or in autism-related gene sets. However, in a patient with high-functioning autism we identified a de novo variant in a canonical splice site of LRP1, a postsynaptic density gene that is a target for fragile X mental retardation protein (FRMP). This de novo variant leads to in-frame skipping of exon 29, removing 2 of 6 blades of the β-propeller domain 4 of LRP1, with putative functional consequences. Large data sets implicate LRP1 across a number of psychiatric disorders: de novo variants are associated with autism-spectrum disorder (p = 0.039) and schizophrenia (p = 0.008) from combined sequencing projects; common variants using genome-wide association study data sets from the Psychiatric Genomics Consortium show gene-based association in schizophrenia (p = 6.6 × E−07) and in a meta-analysis across 7 psychiatric disorders (p = 2.3 × E−03); and the burden of ultra-rare pathogenic variants has been shown to be higher in autism-spectrum disorder (p = 1.2 × E−05), using whole-exome sequencing from 6135 patients with schizophrenia, 1778 patients with autism-spectrum disorder and 7875 controls.

Limitations: We had a limited sample of patients with high-functioning autism, related to difficulty in recruiting probands with high cognitive performance and no family history of psychiatric disorders.

Conclusion: Previous studies and ours suggest an effect of truncating mutations restricted to severe autism-spectrum disorder phenotypes that are associated with intellectual disability. We provide evidence for pleiotropic effects of common and rare variants in the LRP1 gene across psychiatric phenotypes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Alleles
  • Autism Spectrum Disorder / genetics
  • Autistic Disorder / genetics*
  • Databases, Genetic
  • Epilepsy / genetics
  • Exome Sequencing
  • Family
  • Female
  • Gene Regulatory Networks
  • Genetic Pleiotropy
  • Humans
  • Intellectual Disability / genetics
  • Low Density Lipoprotein Receptor-Related Protein-1 / genetics*
  • Male
  • Models, Molecular
  • Mutation
  • RNA Splicing
  • Schizophrenia / genetics
  • Siblings
  • Spain
  • Young Adult

Substances

  • LRP1 protein, human
  • Low Density Lipoprotein Receptor-Related Protein-1