Discovering metabolic disease gene interactions by correlated effects on cellular morphology

Mol Metab. 2019 Jun:24:108-119. doi: 10.1016/j.molmet.2019.03.001. Epub 2019 Mar 13.

Abstract

Objective: Impaired expansion of peripheral fat contributes to the pathogenesis of insulin resistance and Type 2 Diabetes (T2D). We aimed to identify novel disease-gene interactions during adipocyte differentiation.

Methods: Genes in disease-associated loci for T2D, adiposity and insulin resistance were ranked according to expression in human adipocytes. The top 125 genes were ablated in human pre-adipocytes via CRISPR/CAS9 and the resulting cellular phenotypes quantified during adipocyte differentiation with high-content microscopy and automated image analysis. Morphometric measurements were extracted from all images and used to construct morphologic profiles for each gene.

Results: Over 107 morphometric measurements were obtained. Clustering of the morphologic profiles accross all genes revealed a group of 14 genes characterized by decreased lipid accumulation, and enriched for known lipodystrophy genes. For two lipodystrophy genes, BSCL2 and AGPAT2, sub-clusters with PLIN1 and CEBPA identifed by morphological similarity were validated by independent experiments as novel protein-protein and gene regulatory interactions.

Conclusions: A morphometric approach in adipocytes can resolve multiple cellular mechanisms for metabolic disease loci; this approach enables mechanistic interrogation of the hundreds of metabolic disease loci whose function still remains unknown.

Keywords: Functional genomics; Gene discovery; Genetic screen; High content imaging; Insulin resistance; Lipodystrophy; Metabolic syndrome; Type 2 diabetes.

Publication types

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

MeSH terms

  • Acyltransferases / genetics
  • Acyltransferases / metabolism
  • Adipocytes / cytology*
  • Adipocytes / metabolism
  • Adipocytes / pathology
  • Adipogenesis*
  • CCAAT-Enhancer-Binding Proteins / genetics
  • CCAAT-Enhancer-Binding Proteins / metabolism
  • Cells, Cultured
  • Diabetes Mellitus / genetics*
  • Diabetes Mellitus / pathology
  • GTP-Binding Protein gamma Subunits / genetics
  • GTP-Binding Protein gamma Subunits / metabolism
  • Gene Regulatory Networks*
  • HEK293 Cells
  • Humans
  • Insulin Resistance
  • Perilipin-1 / genetics
  • Perilipin-1 / metabolism
  • Phenotype
  • Protein Interaction Maps*
  • Transcriptome

Substances

  • BSCL2 protein, human
  • CCAAT-Enhancer-Binding Proteins
  • CEBPA protein, human
  • GTP-Binding Protein gamma Subunits
  • PLIN1 protein, human
  • Perilipin-1
  • Acyltransferases
  • 2-acylglycerophosphate acyltransferase