Interleukin-17A is dispensable for myocarditis but essential for the progression to dilated cardiomyopathy

Circ Res. 2010 May 28;106(10):1646-55. doi: 10.1161/CIRCRESAHA.109.213157. Epub 2010 Apr 8.

Abstract

Rationale: One-third of myocarditis cases progresses to dilated cardiomyopathy (DCM), but the mechanisms controlling this process are largely unknown. CD4(+) T helper (Th)17 cells have been implicated in the pathogenesis of autoimmune diseases, but the role of Th17-produced cytokines during inflammation-induced cardiac remodeling has not been previously studied.

Objective: We examined the importance of interleukin (IL)-17A in the progression of myocarditis to DCM using a mouse model.

Methods and results: Immunization of mice with myocarditogenic peptide in complete Freund's adjuvant induced the infiltration of IL-17A-producing Th17 cells into the inflamed heart. Unexpectedly, IL-17A-deficient mice developed myocarditis with similar incidence and severity compared to wild-type mice. Additionally, IL-17A deficiency did not ameliorate the severe myocarditis of interferon (IFN)gamma-deficient mice, suggesting that IL-17A plays a minimal role during acute myocarditis. In contrast, IL-17A-deficient mice were protected from postmyocarditis remodeling and did not develop DCM. Flow cytometric and cytokine analysis revealed an important role for IL-17A in heart-specific upregulation of IL-6, TNFalpha, and IL-1beta and the recruitment of CD11b(+) monocyte and Gr1(+) granulocyte populations into the heart. Furthermore, IL-17A-deficient mice had reduced interstitial myocardial fibrosis, downregulated expression of matrix metalloproteinase-2 and -9 and decreased gelatinase activity. Treatment of BALB/c mice with anti-IL-17A monoclonal antibody administered after the onset of myocarditis abrogated myocarditis-induced cardiac fibrosis and preserved ventricular function.

Conclusions: Our findings reveal a critical role for IL-17A in postmyocarditis cardiac remodeling and the progression to DCM. Targeting IL-17A may be an attractive therapy for patients with inflammatory dilated cardiomyopathy.

Publication types

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

MeSH terms

  • Animals
  • Antigens, CD / immunology
  • CD4-Positive T-Lymphocytes / immunology
  • Cardiomyopathies / physiopathology*
  • Chemokines / metabolism
  • Cytokines / metabolism
  • Disease Models, Animal
  • Disease Progression
  • Flow Cytometry
  • Immunization
  • Inflammation / physiopathology
  • Interleukin-17 / deficiency
  • Interleukin-17 / genetics
  • Interleukin-17 / immunology
  • Interleukin-17 / physiology*
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Knockout
  • Mice, Transgenic
  • Myocarditis / physiopathology*
  • Ventricular Function, Left / physiology
  • Ventricular Remodeling / physiology

Substances

  • Antigens, CD
  • Chemokines
  • Cytokines
  • Interleukin-17