Infarcted Myocardium-Primed Dendritic Cells Improve Remodeling and Cardiac Function After Myocardial Infarction by Modulating the Regulatory T Cell and Macrophage Polarization

Circulation. 2017 Apr 11;135(15):1444-1457. doi: 10.1161/CIRCULATIONAHA.116.023106. Epub 2017 Feb 7.

Abstract

Background: Inflammatory responses play a critical role in left ventricular remodeling after myocardial infarction (MI). Tolerogenic dendritic cells (tDCs) can modulate immune responses, inducing regulatory T cells in a number of inflammatory diseases.

Methods: We generated tDCs by treating bone marrow-derived dendritic cells with tumor necrosis factor-α and cardiac lysate from MI mice. We injected MI mice, induced by a ligation of the left anterior descending coronary artery in C57BL/6 mice, twice with tDCs within 24 hours and at 7 days after the ligation.

Results: In vivo cardiac magnetic resonance imaging and ex vivo histology confirmed the beneficial effect on postinfarct left ventricular remodeling in MI mice treated with tDCs. Subcutaneously administered infarct lysate-primed tDCs near the inguinal lymph node migrated to the regional lymph node and induced infarct tissue-specific regulatory T-cell populations in the inguinal and mediastinal lymph nodes, spleen, and infarcted myocardium, indicating that a local injection of tDCs induces a systemic activation of MI-specific regulatory T cells. These events elicited an inflammatory-to-reparative macrophage shift. The altered immune environment in the infarcted heart resulted in a better wound remodeling, preserved left ventricular systolic function after myocardial tissue damage, and improved survival.

Conclusions: This study showed that tDC therapy in a preclinical model of MI was potentially translatable into an antiremodeling therapy for ischemic tissue repair.

Keywords: dendritic cells; heart failure; macrophage; myocardial infarction; regulatory T-cells; ventricular remodeling.

MeSH terms

  • Adoptive Transfer
  • Animals
  • Antigens / immunology
  • Biomarkers
  • Cell Movement
  • Cell- and Tissue-Based Therapy
  • Dendritic Cells / drug effects
  • Dendritic Cells / immunology*
  • Dendritic Cells / metabolism
  • Disease Models, Animal
  • Immunization
  • Lymphocyte Activation
  • Macrophages / immunology*
  • Macrophages / metabolism
  • Magnetic Resonance Imaging
  • Male
  • Mice
  • Myocardial Infarction / diagnosis*
  • Myocardial Infarction / immunology*
  • Myocardial Infarction / physiopathology
  • Myocardial Infarction / therapy
  • Myocardium / immunology
  • Myocardium / pathology
  • Neovascularization, Pathologic
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / metabolism
  • Ventricular Function, Left*
  • Ventricular Remodeling*

Substances

  • Antigens
  • Biomarkers