Human Engineered Heart Muscles Engraft and Survive Long Term in a Rodent Myocardial Infarction Model

Circ Res. 2015 Sep 25;117(8):720-30. doi: 10.1161/CIRCRESAHA.115.306985. Epub 2015 Aug 19.

Abstract

Rationale: Tissue engineering approaches may improve survival and functional benefits from human embryonic stem cell-derived cardiomyocyte transplantation, thereby potentially preventing dilative remodeling and progression to heart failure.

Objective: Assessment of transport stability, long-term survival, structural organization, functional benefits, and teratoma risk of engineered heart muscle (EHM) in a chronic myocardial infarction model.

Methods and results: We constructed EHMs from human embryonic stem cell-derived cardiomyocytes and released them for transatlantic shipping following predefined quality control criteria. Two days of shipment did not lead to adverse effects on cell viability or contractile performance of EHMs (n=3, P=0.83, P=0.87). One month after ischemia/reperfusion injury, EHMs were implanted onto immunocompromised rat hearts to simulate chronic ischemia. Bioluminescence imaging showed stable engraftment with no significant cell loss between week 2 and 12 (n=6, P=0.67), preserving ≤25% of the transplanted cells. Despite high engraftment rates and attenuated disease progression (change in ejection fraction for EHMs, -6.7±1.4% versus control, -10.9±1.5%; n>12; P=0.05), we observed no difference between EHMs containing viable and nonviable human cardiomyocytes in this chronic xenotransplantation model (n>12; P=0.41). Grafted cardiomyocytes showed enhanced sarcomere alignment and increased connexin 43 expression at 220 days after transplantation. No teratomas or tumors were found in any of the animals (n=14) used for long-term monitoring.

Conclusions: EHM transplantation led to high engraftment rates, long-term survival, and progressive maturation of human cardiomyocytes. However, cell engraftment was not correlated with functional improvements in this chronic myocardial infarction model. Most importantly, the safety of this approach was demonstrated by the lack of tumor or teratoma formation.

Keywords: cardiac MRI; cardiac function tests; cell survival; myocardial infarction; myocardial ischemia; tissue engineering; transplantation.

Publication types

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

MeSH terms

  • Animals
  • Biomarkers / metabolism
  • Cell Differentiation
  • Cell Line
  • Cell Survival
  • Connexin 43 / metabolism
  • Disease Models, Animal
  • Embryonic Stem Cells / immunology
  • Embryonic Stem Cells / metabolism
  • Embryonic Stem Cells / transplantation*
  • Graft Survival*
  • Heart Transplantation / adverse effects
  • Heart Transplantation / methods*
  • Heterografts
  • Humans
  • Immunosuppressive Agents / pharmacology
  • Male
  • Myocardial Contraction
  • Myocardial Infarction / immunology
  • Myocardial Infarction / metabolism
  • Myocardial Infarction / pathology
  • Myocardial Infarction / physiopathology
  • Myocardial Infarction / surgery*
  • Myocytes, Cardiac / immunology
  • Myocytes, Cardiac / metabolism
  • Myocytes, Cardiac / pathology
  • Myocytes, Cardiac / transplantation*
  • Papillary Muscles / immunology
  • Papillary Muscles / metabolism
  • Papillary Muscles / pathology
  • Papillary Muscles / physiopathology
  • Papillary Muscles / transplantation*
  • Rats, Nude
  • Rats, Sprague-Dawley
  • Stroke Volume
  • Time Factors
  • Tissue Engineering / methods*
  • Transfection

Substances

  • Biomarkers
  • Connexin 43
  • GJA1 protein, human
  • Immunosuppressive Agents