Interleukin-10 treatment attenuates pressure overload-induced hypertrophic remodeling and improves heart function via signal transducers and activators of transcription 3-dependent inhibition of nuclear factor-κB

Circulation. 2012 Jul 24;126(4):418-29. doi: 10.1161/CIRCULATIONAHA.112.112185. Epub 2012 Jun 15.

Abstract

Background: Inflammation plays a critical role in adverse cardiac remodeling and heart failure. Therefore, approaches geared toward inhibiting inflammation may provide therapeutic benefits. We tested the hypotheses that genetic deletion of interleukin-10 (IL-10), a potent antiinflammatory cytokine, exacerbates pressure overload-induced adverse cardiac remodeling and hypertrophy and that IL-10 therapy inhibits this pathology.

Methods and results: Cardiac hypertrophy was induced in wild-type and IL-10 knockout mice by isoproterenol (ISO) infusion. ISO-induced left ventricular dysfunction and hypertrophic remodeling, including fibrosis and fetal gene expression, were further exaggerated in knockout mice compared with wild-type mice. Systemic recombinant mouse IL-10 administration markedly improved left ventricular function and not only inhibited but also reversed ISO-induced cardiac remodeling. Intriguingly, a very similar cardioprotective response of IL-10 was found in transverse aortic constriction-induced hypertrophy and heart failure models. In neonatal rat ventricular myocytes and H9c2 myoblasts, ISO activated nuclear factor-κB and inhibited signal transducers and activators of transcription 3 (STAT3) phosphorylation. Interestingly, IL-10 suppressed ISO-induced nuclear factor-κB activation and attenuated STAT3 inhibition. Moreover, pharmacological and genetic inhibition of STAT3 reversed the protective effects of IL-10, whereas ectopic expression of constitutively active STAT3 mimicked the IL-10 responses on the ISO effects, confirming that the IL-10-mediated inhibition of nuclear factor-κB is STAT3 dependent.

Conclusion: Taken together, our results suggest IL-10 treatment as a potential therapeutic approach to limit the progression of pressure overload-induced adverse cardiac remodeling.

Publication types

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

MeSH terms

  • Animals
  • Cardiomegaly / chemically induced
  • Cardiomegaly / drug therapy*
  • Cardiomegaly / metabolism
  • Disease Models, Animal
  • Disease Susceptibility
  • Fibrosis
  • Interleukin-10 / genetics
  • Interleukin-10 / pharmacology*
  • Interleukin-10 / therapeutic use*
  • Isoproterenol / adverse effects
  • Isoproterenol / pharmacology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Myoblasts, Cardiac / cytology
  • Myoblasts, Cardiac / drug effects
  • Myoblasts, Cardiac / metabolism
  • Myocardium / pathology
  • NF-kappa B / antagonists & inhibitors*
  • NF-kappa B / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction / drug effects
  • Signal Transduction / physiology
  • Ventricular Dysfunction, Left / drug therapy*
  • Ventricular Dysfunction, Left / pathology
  • Ventricular Dysfunction, Left / physiopathology
  • Ventricular Remodeling / drug effects*
  • Ventricular Remodeling / physiology

Substances

  • NF-kappa B
  • STAT3 Transcription Factor
  • Stat3 protein, mouse
  • Interleukin-10
  • Isoproterenol