Autologous mesenchymal stem cells mobilize cKit+ and CD133+ bone marrow progenitor cells and improve regional function in hibernating myocardium

Circ Res. 2011 Oct 14;109(9):1044-54. doi: 10.1161/CIRCRESAHA.111.245969. Epub 2011 Sep 1.

Abstract

Rationale: Mesenchymal stem cells (MSCs) improve function after infarction, but their mechanism of action remains unclear, and the importance of reduced scar volume, cardiomyocyte proliferation, and perfusion is uncertain.

Objective: The present study was conducted to test the hypothesis that MSCs mobilize bone marrow progenitor cells and improve function by stimulating myocyte proliferation in collateral-dependent hibe rnating myocardium.

Methods and results: Swine with chronic hibernating myocardium received autologous intracoronary MSCs (icMSCs; ≈44 ×10(6) cells, n = 10) 4 months after instrumentation and were studied up to 6 weeks later. Physiological and immunohistochemical findings were compared with untreated hibernating animals (n = 7), sham-normal animals (n = 5), and icMSC-treated sham-normal animals (n = 6). In hibernating myocardium, icMSCs increased function (percent wall thickening of the left anterior descending coronary artery 24 ± 4% to 43 ± 5%, P < 0.05), although left anterior descending coronary artery flow reserve (adenosine/rest) remained critically impaired (1.2 ± 0.1 versus 1.2 ± 0.1). Circulating cKit+ and CD133+ bone marrow progenitor cells increased transiently after icMSC administration, with a corresponding increase in myocardial cKit+/CD133+ and cKit+/CD133- bone marrow progenitor cells (total cKit+ from 223 ± 49 to 4415 ± 866/10(6) cardiomyocytes, P < 0.05). In hibernating hearts, icMSCs increased Ki67+ cardiomyocytes (from 410 ± 83 to 2460 ± 610/10(6) nuclei, P < 0.05) and phospho-histone H3-positive cardiomyocytes (from 9 ± 5 to 116 ± 12/10(6) nuclei, P < 0.05). Myocyte nuclear number (from 75 336 ± 5037 to 114 424 ± 9564 nuclei/mm3, P < 0.01) and left ventricular mass (from 2.5 ± 0.1 to 2.8 ± 0.1 g/kg, P < 0.05) increased, yet myocytes were smaller (14.5 ± 0.4 versus 16.5 ± 0.4 μm, P < 0.05), which supports endogenous cardiomyocyte proliferation. In sham-normal animals, icMSCs increased myocardial bone marrow progenitor cells with no effect on myocyte proliferation or regional function.

Conclusions: Our results indicate that icMSCs improve function in hibernating myocardium independent of coronary flow or reduced scar volume. This arises from stimulation of myocyte proliferation with increases in cKit+/CD133+ bone marrow progenitor cells and cKit+/CD133- resident stem cells, which increase myocyte number and reduce cellular hypertrophy.

Publication types

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

MeSH terms

  • AC133 Antigen
  • Animals
  • Antigens, CD / metabolism*
  • Bone Marrow Cells / cytology
  • Bone Marrow Cells / metabolism*
  • Cell Cycle / physiology
  • Cell Movement / physiology
  • Cell Proliferation
  • Chemokines / metabolism
  • Glycoproteins / metabolism*
  • Heart / physiology*
  • Mesenchymal Stem Cell Transplantation
  • Mesenchymal Stem Cells / cytology
  • Mesenchymal Stem Cells / physiology*
  • Models, Animal
  • Myocardial Stunning / physiopathology*
  • Myocardial Stunning / therapy
  • Myocytes, Cardiac / pathology
  • Neovascularization, Physiologic / physiology
  • Peptides / metabolism*
  • Proto-Oncogene Proteins c-kit / metabolism*
  • Stem Cells / cytology
  • Stem Cells / metabolism*
  • Swine

Substances

  • AC133 Antigen
  • Antigens, CD
  • Chemokines
  • Glycoproteins
  • Peptides
  • Proto-Oncogene Proteins c-kit