Genome Editing in hPSCs Reveals GATA6 Haploinsufficiency and a Genetic Interaction with GATA4 in Human Pancreatic Development

Cell Stem Cell. 2017 May 4;20(5):675-688.e6. doi: 10.1016/j.stem.2017.01.001. Epub 2017 Feb 9.

Abstract

Human disease phenotypes associated with haploinsufficient gene requirements are often not recapitulated well in animal models. Here, we have investigated the association between human GATA6 haploinsufficiency and a wide range of clinical phenotypes that include neonatal and adult-onset diabetes using CRISPR (clustered regularly interspaced short palindromic repeat)/Cas9-mediated genome editing coupled with human pluripotent stem cell (hPSC) directed differentiation. We found that loss of one GATA6 allele specifically affects the differentiation of human pancreatic progenitors from the early PDX1+ stage to the more mature PDX1+NKX6.1+ stage, leading to impaired formation of glucose-responsive β-like cells. In addition to this GATA6 haploinsufficiency, we also identified dosage-sensitive requirements for GATA6 and GATA4 in the formation of both definitive endoderm and pancreatic progenitor cells. Our work expands the application of hPSCs from studying the impact of individual gene loci to investigation of multigenic human traits, and it establishes an approach for identifying genetic modifiers of human disease.

Keywords: CRISPR/Cas9 genome editing; GATA6 and GATA4; definitive endoderm; genetic modifier; haploinsufficiency; human embryonic stem cells; human pluripotent stem cells disease modeling; insulin producing pancreatic beta cells; pancreatic agenesis and neonatal diabetes; pancreatic progenitor.

MeSH terms

  • Animals
  • Cell Differentiation / genetics
  • Cell Differentiation / physiology
  • Cell Line
  • Fluorescent Antibody Technique
  • GATA4 Transcription Factor / genetics*
  • GATA6 Transcription Factor / genetics*
  • Gene Editing / methods*
  • Haploinsufficiency / genetics
  • Haploinsufficiency / physiology
  • Humans
  • Male
  • Pancreas / cytology
  • Pancreas / metabolism
  • Pluripotent Stem Cells / cytology*
  • Pluripotent Stem Cells / metabolism*

Substances

  • GATA4 Transcription Factor
  • GATA4 protein, human
  • GATA6 Transcription Factor
  • GATA6 protein, human