Upregulation of the JAK-STAT pathway promotes maturation of human embryonic stem cell-derived cardiomyocytes

Stem Cell Reports. 2021 Dec 14;16(12):2928-2941. doi: 10.1016/j.stemcr.2021.10.009. Epub 2021 Nov 11.

Abstract

The immature characteristics and metabolic phenotypes of human pluripotent stem cell-derived cardiomyocytes (hPSC-CMs) restrict their applications for disease modeling, drug discovery, and cell-based therapy. Leveraging on the metabolic shifts from glycolysis to fatty acid oxidation as CMs mature, a human hexokinase1-GFP metabolic reporter cell line (H7 HK1-GFP) was generated to facilitate the isolation of fetal or more matured hPSC-CMs. RNA sequencing of fetal versus more matured CMs uncovered a potential role of interferon-signaling pathway in regulating CM maturation. Indeed, IFN-γ-treated CMs resulted in an upregulation of the JAK-STAT pathway, which was found to be associated with increased expression of CM maturation genes, shift from MYH6 to MYH7 expression, and improved sarcomeric structure. Functionally, IFN-γ-treated CMs exhibited a more matured electrophysiological profile, such as increased calcium dynamics and action potential upstroke velocity, demonstrated through calcium imaging and MEA. Expectedly, the functional improvements were nullified with a JAK-STAT inhibitor, ruxolitinib.

Keywords: JAK-STAT pathway; RNA sequencing; cardiomyocyte maturation; electrophysiology; stem cell differentiation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • CRISPR-Cas Systems / genetics
  • Cell Differentiation* / drug effects
  • Cell Line
  • Electrophysiological Phenomena / drug effects
  • Genes, Reporter
  • Green Fluorescent Proteins / metabolism
  • Human Embryonic Stem Cells / cytology*
  • Human Embryonic Stem Cells / drug effects
  • Human Embryonic Stem Cells / metabolism*
  • Humans
  • Interferon-gamma / metabolism
  • Interferon-gamma / pharmacology
  • Janus Kinases / metabolism*
  • Myocytes, Cardiac / cytology*
  • STAT Transcription Factors / metabolism*
  • Signal Transduction* / drug effects
  • Up-Regulation* / drug effects

Substances

  • STAT Transcription Factors
  • Green Fluorescent Proteins
  • Interferon-gamma
  • Janus Kinases