Sca-1+ cardiac fibroblasts promote development of heart failure

Eur J Immunol. 2018 Sep;48(9):1522-1538. doi: 10.1002/eji.201847583. Epub 2018 Jul 18.

Abstract

The causative effect of GM-CSF produced by cardiac fibroblasts to development of heart failure has not been shown. We identified the pathological GM-CSF-producing cardiac fibroblast subset and the specific deletion of IL-17A signaling to these cells attenuated cardiac inflammation and heart failure. We describe here the CD45- CD31- CD29+ mEF-SK4+ PDGFRα+ Sca-1+ periostin+ (Sca-1+ ) cardiac fibroblast subset as the main GM-CSF producer in both experimental autoimmune myocarditis and myocardial infarction mouse models. Specific ablation of IL-17A signaling to Sca-1+ periostin+ cardiac fibroblasts (PostnCre Il17rafl/fl ) protected mice from post-infarct heart failure and death. Moreover, PostnCre Il17rafl/fl mice had significantly fewer GM-CSF-producing Sca-1+ cardiac fibroblasts and inflammatory Ly6Chi monocytes in the heart. Sca-1+ cardiac fibroblasts were not only potent GM-CSF producers, but also exhibited plasticity and switched their cytokine production profiles depending on local microenvironments. Moreover, we also found GM-CSF-positive cardiac fibroblasts in cardiac biopsy samples from heart failure patients of myocarditis or ischemic origin. Thus, this is the first identification of a pathological GM-CSF-producing cardiac fibroblast subset in human and mice hearts with myocarditis and ischemic cardiomyopathy. Sca-1+ cardiac fibroblasts direct the type of immune cells infiltrating the heart during cardiac inflammation and drive the development of heart failure.

Keywords: Fibroblasts; GM-CSF; Heart failure; IL-17; Myocarditis.

Publication types

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

MeSH terms

  • Animals
  • Ataxin-1 / genetics*
  • Cells, Cultured
  • Chemokine CCL2 / biosynthesis
  • Fibroblasts / metabolism*
  • Granulocyte-Macrophage Colony-Stimulating Factor / metabolism*
  • Heart Failure / pathology*
  • Humans
  • Interleukin-17 / metabolism
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Myocardial Infarction / pathology*
  • Myocarditis / pathology*
  • Myocytes, Cardiac / metabolism*

Substances

  • Ataxin-1
  • Atxn1 protein, mouse
  • CCL2 protein, human
  • Chemokine CCL2
  • Il17a protein, mouse
  • Interleukin-17
  • Granulocyte-Macrophage Colony-Stimulating Factor