Functional impairment of human resident cardiac stem cells by the cardiotoxic antineoplastic agent trastuzumab

Stem Cells Transl Med. 2012 Apr;1(4):289-97. doi: 10.5966/sctm.2011-0016. Epub 2012 Apr 10.

Abstract

Trastuzumab (TZM), a monoclonal antibody against the ERBB2 protein, increases survival in ERBB2-positive breast cancer patients. Its clinical use, however, is limited by cardiotoxicity. We sought to evaluate whether TZM cardiotoxicity involves inhibition of human adult cardiac-derived stem cells, in addition to previously reported direct adverse effects on cardiomyocytes. To test this idea, we exposed human cardiosphere-derived cells (hCDCs), a natural mixture of cardiac stem cells and supporting cells that has been shown to exert potent regenerative effects, to TZM and tested the effects in vitro and in vivo. We found that ERBB2 mRNA and protein are expressed in hCDCs at levels comparable to those in human myocardium. Although clinically relevant concentrations of TZM had no effect on proliferation, apoptosis, or size of the c-kit-positive hCDC subpopulation, in vitro assays demonstrated diminished potential for cardiogenic differentiation and impaired ability to form microvascular networks in TZM-treated cells. The functional benefit of hCDCs injected into the border zone of acutely infarcted mouse hearts was abrogated by TZM: infarcted animals treated with TZM + hCDCs had a lower ejection fraction, thinner infarct scar, and reduced capillary density in the infarct border zone compared with animals that received hCDCs alone (n = 12 per group). Collectively, these results indicate that TZM inhibits the cardiomyogenic and angiogenic capacities of hCDCs in vitro and abrogates the morphological and functional benefits of hCDC transplantation in vivo. Thus, TZM impairs the function of human resident cardiac stem cells, potentially contributing to TZM cardiotoxicity.

Publication types

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

MeSH terms

  • Animals
  • Antibodies, Monoclonal, Humanized / adverse effects*
  • Antibodies, Monoclonal, Humanized / therapeutic use
  • Antineoplastic Agents / adverse effects*
  • Antineoplastic Agents / therapeutic use
  • Cardiotoxins / adverse effects*
  • Cardiotoxins / therapeutic use
  • Cell Differentiation / drug effects*
  • Cell Line, Tumor
  • Female
  • Gene Expression Regulation / drug effects
  • Humans
  • Male
  • Mice
  • Mice, SCID
  • Muscle Proteins / antagonists & inhibitors
  • Muscle Proteins / biosynthesis
  • Myocardial Infarction / metabolism
  • Myocardial Infarction / pathology
  • Myocardial Infarction / therapy
  • Myocardium / metabolism*
  • Myocardium / pathology
  • RNA, Messenger / biosynthesis
  • Receptor, ErbB-2 / antagonists & inhibitors
  • Receptor, ErbB-2 / biosynthesis
  • Regeneration / drug effects*
  • Stem Cell Transplantation
  • Stem Cells / metabolism*
  • Stem Cells / pathology
  • Transplantation, Heterologous
  • Trastuzumab

Substances

  • Antibodies, Monoclonal, Humanized
  • Antineoplastic Agents
  • Cardiotoxins
  • Muscle Proteins
  • RNA, Messenger
  • ERBB2 protein, human
  • Receptor, ErbB-2
  • Trastuzumab