Antibodies aggravate the development of ischemic heart failure

Am J Physiol Heart Circ Physiol. 2018 Nov 1;315(5):H1358-H1367. doi: 10.1152/ajpheart.00144.2018. Epub 2018 Aug 10.

Abstract

Heart-specific antibodies have been widely associated with myocardial infarction (MI). However, it remains unclear whether autoantibodies mediate disease progression or are a byproduct of cardiac injury. To disambiguate the role of immunoglobulins in MI, we characterized the development of ischemic heart failure in agammaglobulinemic mice (AID-/-μS-/-). Although these animals can produce functional B cells, they cannot synthesize secretory IgM (μS-/-) or perform Ig class switching (AID-/-), leading to complete antibody deficiency. Agammaglobulinemia did not affect overall post-MI survival but resulted in a significant reduction in infarct size. Echocardiographic analyses showed that, compared with wild-type infarcted control mice, AID-/-μS-/- mice exhibited improved cardiac function and reduced remodeling on day 56 post-MI. These differences remained significant even after animals with matched infarct sizes were compared. Infarcted AID-/-μS-/- mice also showed reduced myocardial expression levels of transcripts known to promote adverse remodeling, such as matrix metalloproteinase-9, collagen type I a1, collagen type III a1, and IL-6. An unbiased screening of the heart reactivity potential in the plasma of wild-type MI animals revealed the presence of antibodies that target the myocardial scar and collagenase-sensitive epitopes. Moreover, we found that IgG accumulated within the scar tissues of infarcted mice and remained in close proximity with cells expressing Fcγ receptors (CD16/32), suggesting the existence of an in situ IgG-Fcγ receptor axis. Collectively, our study results confirm that antibodies contribute to ischemic heart failure progression and provide novel insights into the mechanisms underlying this phenomenon. NEW & NOTEWORTHY Our study sheds some light on the long-standing debate over the relevance of autoantibodies in heart failure and might stimulate future research in the field. The observation of extracellular matrix-specific antibodies and the detection of Fcγ receptor-expressing cells within the scar provide novel insights into the mechanisms by which antibodies may contribute to adverse remodeling.

Keywords: antibodies; heart failure; myocardial infarction; remodeling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Agammaglobulinemia / complications
  • Agammaglobulinemia / genetics
  • Agammaglobulinemia / immunology*
  • Agammaglobulinemia / metabolism
  • Animals
  • Autoantibodies / immunology*
  • Autoantibodies / metabolism
  • Disease Models, Animal
  • Extracellular Matrix / immunology
  • Extracellular Matrix / metabolism
  • Extracellular Matrix / pathology
  • Fibrosis
  • Heart Failure / immunology
  • Heart Failure / metabolism
  • Heart Failure / pathology
  • Heart Failure / prevention & control*
  • Immunoglobulin Class Switching* / genetics
  • Immunoglobulin M / genetics
  • Immunoglobulin M / immunology*
  • Immunoglobulin M / metabolism
  • Male
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Myocardial Infarction / complications
  • Myocardial Infarction / immunology*
  • Myocardial Infarction / metabolism
  • Myocardial Infarction / pathology
  • Myocarditis / immunology
  • Myocarditis / metabolism
  • Myocarditis / pathology
  • Myocarditis / prevention & control*
  • Myocardium / immunology*
  • Myocardium / metabolism
  • Myocardium / pathology
  • Receptors, IgG / immunology
  • Receptors, IgG / metabolism
  • Ventricular Function, Left
  • Ventricular Remodeling

Substances

  • Autoantibodies
  • Immunoglobulin M
  • Receptors, IgG
  • secretory IgM