Interrogation of the Atherosclerosis-Associated SORT1 (Sortilin 1) Locus With Primary Human Hepatocytes, Induced Pluripotent Stem Cell-Hepatocytes, and Locus-Humanized Mice

Arterioscler Thromb Vasc Biol. 2018 Jan;38(1):76-82. doi: 10.1161/ATVBAHA.117.310103. Epub 2017 Nov 2.

Abstract

Objective: The noncoding single-nucleotide polymorphism rs12740374 has been hypothesized to be the causal variant responsible for liver-specific modulation of SORT1(sortilin 1) expression (ie, expression quantitative trait locus) and, by extension, the association of the SORT1 locus on human chromosome 1p13 with low-density lipoprotein cholesterol levels and coronary heart disease. The goals of this study were to compare 3 different hepatocyte models in demonstrating that the rs12740374 minor allele sequence is responsible for transcriptional activation of SORT1 expression.

Approach and results: We found that although primary human hepatocytes of varied rs12740374 genotypes strongly replicated the SORT1 expression quantitative trait locus observed previously in whole-liver samples, a population cohort of induced pluripotent stem cell-derived hepatocyte-like cells poorly replicated the expression quantitative trait locus. In primary human hepatocytes from multiple individuals heterozygous at rs12740374, we used CRISPR-Cas9 (clustered regularly interspaced short palindromic repeats-associated 9) to specifically target the rs12740374 minor allele sequence ex vivo, resulting in a reproducible reduction in SORT1 expression. We generated a locus-humanized transgenic mouse with a bacterial artificial chromosome bearing the human SORT1 locus with the rs12740374 minor allele. In this mouse model, we used CRISPR-Cas9 to target the rs12740374 minor allele sequence in the liver in vivo, resulting in a substantial reduction of hepatic SORT1 expression.

Conclusions: The rs12740374 minor allele sequence enhances SORT1 expression in hepatocytes. CRISPR-Cas9 can be used in primary human hepatocytes ex vivo and locus-humanized mice in vivo to interrogate the function of noncoding regulatory regions. Induced pluripotent stem cell-derived hepatocyte-like cells experience limitations that prevent faithful modelling of some hepatocyte expression quantitative trait loci.

Keywords: animals; coronary disease; gene expression; genotype; liver.

Publication types

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

MeSH terms

  • Adaptor Proteins, Vesicular Transport / genetics
  • Adaptor Proteins, Vesicular Transport / metabolism*
  • Animals
  • Atherosclerosis / genetics
  • Atherosclerosis / metabolism*
  • Atherosclerosis / pathology
  • CRISPR-Cas Systems
  • Cells, Cultured
  • Disease Models, Animal
  • Gene Editing / methods
  • Gene Expression Regulation
  • Genetic Predisposition to Disease
  • Hepatocytes / metabolism*
  • Hepatocytes / pathology
  • Heterozygote
  • Humans
  • Induced Pluripotent Stem Cells / metabolism*
  • Induced Pluripotent Stem Cells / pathology
  • Mice, Transgenic
  • Phenotype
  • Polymorphism, Single Nucleotide
  • Quantitative Trait Loci
  • Transcription, Genetic

Substances

  • Adaptor Proteins, Vesicular Transport
  • sortilin