Modulation of subsets of cardiac B lymphocytes improves cardiac function after acute injury

JCI Insight. 2018 Jun 7;3(11):e120137. doi: 10.1172/jci.insight.120137.

Abstract

Despite the long-standing recognition that the immune response to acute myocardial injury contributes to adverse left ventricular (LV) remodeling, it has not been possible to effectively target this clinically. Using 2 different in vivo models of acute myocardial injury, we show that pirfenidone confers beneficial effects in the murine heart through an unexpected mechanism that depends on cardiac B lymphocytes. Naive hearts contained a large population of CD19+CD11b-CD23-CD21-IgD+IgMlo lymphocytes, and 2 smaller populations of CD19+CD11b+ B1a and B1b cells. In response to tissue injury, there was an increase in neutrophils, monocytes, macrophages, as well as an increase in CD19+ CD11b- B lymphocytes. Treatment with pirfenidone had no effect on the number of neutrophils, monocytes, or macrophages, but decreased CD19+CD11b- lymphocytes. B cell depletion abrogated the beneficial effects of pirfenidone. In vitro studies demonstrated that stimulation with lipopolysaccharide and extracts from necrotic cells activated CD19+ lymphocytes through a TIRAP-dependent pathway. Treatment with pirfenidone attenuated this activation of B cells. These findings reveal a previously unappreciated complexity of myocardial B lymphocytes within the inflammatory infiltrate triggered by cardiac injury and suggest that pirfenidone exerts beneficial effects in the heart through a unique mechanism that involves modulation of cardiac B lymphocytes.

Keywords: B cells; Cardiology; Heart failure.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • B-Lymphocyte Subsets / drug effects
  • B-Lymphocyte Subsets / immunology*
  • Diphtheria Toxin / administration & dosage
  • Diphtheria Toxin / immunology
  • Disease Models, Animal
  • Female
  • Heart Ventricles / drug effects*
  • Heart Ventricles / immunology
  • Heart Ventricles / pathology
  • Heart Ventricles / physiopathology
  • Humans
  • Lipopolysaccharides / administration & dosage
  • Lipopolysaccharides / immunology
  • Lymphocyte Activation / drug effects
  • Lymphocyte Depletion / methods
  • Mice
  • Myocardial Infarction / drug therapy
  • Myocardial Infarction / immunology*
  • Myocardial Infarction / pathology
  • Myocardial Infarction / physiopathology
  • Myocardium / cytology
  • Myocardium / immunology
  • Myocardium / pathology
  • Pyridones / administration & dosage*
  • Reperfusion Injury / immunology
  • Reperfusion Injury / pathology
  • Reperfusion Injury / physiopathology
  • Ventricular Remodeling / drug effects*
  • Ventricular Remodeling / immunology

Substances

  • Diphtheria Toxin
  • Lipopolysaccharides
  • Pyridones
  • pirfenidone