A Scalable Approach Reveals Functional Responses of iPSC Cardiomyocyte 3D Spheroids

SLAS Discov. 2021 Mar;26(3):352-363. doi: 10.1177/2472555220975332. Epub 2020 Dec 7.

Abstract

Cardiomyocytes (CMs) derived from induced pluripotent stem cells (iPSCs) provide an in vitro model of the human myocardium. Complex 3D scaffolded culture methods improve the phenotypical maturity of iPSC-CMs, although typically at the expense of throughput. We have developed a novel, scalable approach that enables the use of iPSC-CM 3D spheroid models in a label-free readout system in a standard 96-well plate-based format. Spheroids were accurately positioned onto recording electrodes using a magnetic gold-iron oxide nanoparticle approach. Remarkably, both contractility (impedance) and extracellular field potentials (EFPs) could be detected from the actively beating spheroids over long durations and after automated dosing with pharmacological agents. The effects on these parameters of factors, such as co-culture (including human primary cardiac fibroblasts), extracellular buffer composition, and electrical pacing, were investigated. Beat amplitudes were increased greater than 15-fold by co-culture with fibroblasts. Optimization of extracellular Ca2+ fluxes and electrical pacing promoted the proper physiological response to positive inotropic agonists of increased beat amplitude (force) rather than the increased beat rate often observed in iPSC-CM studies. Mechanistically divergent repolarizations in different spheroid models were indicated by their responses to BaCl2 compared with E-4031. These studies demonstrate a new method that enables the pharmacological responses of 3D iPSC-CM spheroids to be determined in a label-free, standardized, 96-well plate-based system. This approach could have discovery applications across cardiovascular efficacy and safety, where parameters typically sought as readouts of iPSC-CM maturity or physiological relevance have the potential to improve assay predictivity.

Keywords: cardiomyocyte; co-culture; contractility; screening; stem cell.

MeSH terms

  • Anti-Arrhythmia Agents / pharmacology*
  • Barium Compounds / pharmacology
  • Biological Assay
  • Calcium / metabolism
  • Cell Differentiation
  • Chlorides / pharmacology
  • Coculture Techniques
  • Ferric Compounds / chemistry
  • Fibroblasts / cytology
  • Fibroblasts / drug effects*
  • Fibroblasts / metabolism
  • Gold / chemistry
  • Humans
  • Induced Pluripotent Stem Cells / cytology
  • Induced Pluripotent Stem Cells / drug effects
  • Induced Pluripotent Stem Cells / metabolism
  • Ion Transport
  • Metal Nanoparticles / chemistry
  • Metal Nanoparticles / ultrastructure
  • Models, Biological
  • Myocardial Contraction / drug effects*
  • Myocardial Contraction / physiology
  • Myocardium / cytology
  • Myocardium / metabolism
  • Myocytes, Cardiac / cytology
  • Myocytes, Cardiac / drug effects*
  • Myocytes, Cardiac / metabolism
  • Piperidines / pharmacology*
  • Pyridines / pharmacology*
  • Spheroids, Cellular / cytology
  • Spheroids, Cellular / drug effects*
  • Spheroids, Cellular / metabolism

Substances

  • Anti-Arrhythmia Agents
  • Barium Compounds
  • Chlorides
  • Ferric Compounds
  • Piperidines
  • Pyridines
  • barium chloride
  • E 4031
  • ferric oxide
  • Gold
  • Calcium