Functional integration of electrically active cardiac derivatives from genetically engineered human embryonic stem cells with quiescent recipient ventricular cardiomyocytes: insights into the development of cell-based pacemakers

Circulation. 2005 Jan 4;111(1):11-20. doi: 10.1161/01.CIR.0000151313.18547.A2. Epub 2004 Dec 20.

Abstract

Background: Human embryonic stem cells (hESCs) derived from blastocysts can propagate indefinitely in culture while maintaining pluripotency, including the ability to differentiate into cardiomyocytes (CMs); therefore, hESCs may provide an unlimited source of human CMs for cell-based therapies. Although CMs can be derived from hESCs ex vivo, it remains uncertain whether a functional syncytium can be formed between donor and recipient cells after engraftment.

Methods and results: Using a combination of electrophysiological and imaging techniques, here we demonstrate that electrically active, donor CMs derived from hESCs that had been stably genetically engineered by a recombinant lentivirus can functionally integrate with otherwise-quiescent, recipient, ventricular CMs to induce rhythmic electrical and contractile activities in vitro. The integrated syncytium was responsive to the beta-adrenergic agonist isoproterenol as well as to other pharmacological agents such as lidocaine and ZD7288. Similarly, a functional hESC-derived pacemaker could be implanted in the left ventricle in vivo. Detailed optical mapping of the epicardial surface of guinea pig hearts transplanted with hESC-derived CMs confirmed the successful spread of membrane depolarization from the site of injection to the surrounding myocardium.

Conclusions: We conclude that electrically active, hESC-derived CMs are capable of actively pacing quiescent, recipient, ventricular CMs in vitro and ventricular myocardium in vivo. Our results may lead to an alternative or a supplemental method for correcting defects in cardiac impulse generation, such as cell-based pacemakers.

Publication types

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

MeSH terms

  • Action Potentials
  • Adrenergic beta-Agonists / pharmacology
  • Animals
  • Cell Differentiation
  • Cell Fusion
  • Cells, Cultured / cytology
  • Cells, Cultured / physiology
  • Defective Viruses / genetics
  • Defective Viruses / physiology
  • Electrophysiology
  • Female
  • Genes, Reporter
  • Genetic Vectors / pharmacology*
  • Giant Cells / cytology
  • Giant Cells / drug effects
  • Green Fluorescent Proteins / analysis
  • Green Fluorescent Proteins / genetics
  • Guinea Pigs
  • HIV-1 / genetics
  • HIV-1 / physiology
  • Heart / physiology
  • Heart Conduction System / cytology
  • Heart Conduction System / physiology
  • Heart Ventricles / cytology
  • Humans
  • Isoproterenol / pharmacology
  • Lidocaine / pharmacology
  • Mice
  • Myocardial Contraction / drug effects
  • Myocytes, Cardiac / cytology*
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / physiology
  • Myocytes, Cardiac / transplantation
  • Organ Culture Techniques
  • Pericardium / physiology
  • Pluripotent Stem Cells / cytology*
  • Pluripotent Stem Cells / physiology
  • Pyrimidines / pharmacology
  • Rats
  • Transduction, Genetic

Substances

  • Adrenergic beta-Agonists
  • Pyrimidines
  • ICI D2788
  • Green Fluorescent Proteins
  • Lidocaine
  • Isoproterenol