Rapid and quantitative functional interrogation of human enhancer variant activity in live mice

Nat Commun. 2025 Jan 6;16(1):409. doi: 10.1038/s41467-024-55500-7.

Abstract

Functional analysis of non-coding variants associated with congenital disorders remains challenging due to the lack of efficient in vivo models. Here we introduce dual-enSERT, a robust Cas9-based two-color fluorescent reporter system which enables rapid, quantitative comparison of enhancer allele activities in live mice in less than two weeks. We use this technology to examine and measure the gain- and loss-of-function effects of enhancer variants previously linked to limb polydactyly, autism spectrum disorder, and craniofacial malformation. By combining dual-enSERT with single-cell transcriptomics, we characterise gene expression in cells where the enhancer is normally and ectopically active, revealing candidate pathways that may lead to enhancer misregulation. Finally, we demonstrate the widespread utility of dual-enSERT by testing the effects of fifteen previously uncharacterised rare and common non-coding variants linked to neurodevelopmental disorders. In doing so we identify variants that reproducibly alter the in vivo activity of OTX2 and MIR9-2 brain enhancers, implicating them in autism. Dual-enSERT thus allows researchers to go from identifying candidate enhancer variants to analysis of comparative enhancer activity in live embryos in under two weeks.

MeSH terms

  • Alleles
  • Animals
  • Autism Spectrum Disorder / genetics
  • Autism Spectrum Disorder / metabolism
  • Brain / metabolism
  • CRISPR-Cas Systems
  • Craniofacial Abnormalities / genetics
  • Enhancer Elements, Genetic* / genetics
  • Female
  • Genes, Reporter
  • Genetic Variation
  • Humans
  • Male
  • Mice
  • MicroRNAs / genetics
  • MicroRNAs / metabolism
  • Otx Transcription Factors* / genetics
  • Otx Transcription Factors* / metabolism
  • Single-Cell Analysis

Substances

  • Otx Transcription Factors
  • MicroRNAs
  • Otx2 protein, mouse