Cofilin-2 phosphorylation and sequestration in myocardial aggregates: novel pathogenetic mechanisms for idiopathic dilated cardiomyopathy

J Am Coll Cardiol. 2015 Mar 31;65(12):1199-1214. doi: 10.1016/j.jacc.2015.01.031.

Abstract

Background: Recently, tangles and plaque-like aggregates have been identified in certain cases of dilated cardiomyopathy (DCM), traditionally labeled idiopathic (iDCM), where there is no specific diagnostic test or targeted therapy. This suggests a potential underlying cause for some of the iDCM cases. [Corrected]

Objectives: This study sought to identify the make-up of myocardial aggregates to understand the molecular mechanisms of these cases of DCM; this strategy has been central to understanding Alzheimer's disease.

Methods: Aggregates were extracted from human iDCM samples with high congophilic reactivity (an indication of plaque presence), and the findings were validated in a larger cohort of samples. We tested the expression, distribution, and activity of cofilin in human tissue and generated a cardiac-specific knockout mouse model to investigate the functional impact of the human findings. We also modeled cofilin inactivity in vitro by using pharmacological and genetic gain- and loss-of-function approaches.

Results: Aggregates in human myocardium were enriched for cofilin-2, an actin-depolymerizing protein known to participate in neurodegenerative diseases and nemaline myopathy. Cofilin-2 was predominantly phosphorylated, rendering it inactive. Cardiac-specific haploinsufficiency of cofilin-2 in mice recapitulated the human disease's morphological, functional, and structural phenotype. Pharmacological stimulation of cofilin-2 phosphorylation and genetic overexpression of the phosphomimetic protein promoted the accumulation of "stress-like" fibers and severely impaired cardiomyocyte contractility.

Conclusions: Our study provides the first biochemical characterization of prefibrillar myocardial aggregates in humans and the first report to link cofilin-2 to cardiomyopathy. The findings suggest a common pathogenetic mechanism connecting certain iDCMs and other chronic degenerative diseases, laying the groundwork for new therapeutic strategies.

Keywords: adenovirus; heart failure; nemaline.

Publication types

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

MeSH terms

  • Adult
  • Aged
  • Animals
  • Cardiomyopathy, Dilated / genetics*
  • Cardiomyopathy, Dilated / physiopathology*
  • Cardiomyopathy, Dilated / surgery
  • Cofilin 2 / genetics*
  • Cofilin 2 / metabolism
  • Female
  • Frozen Sections
  • Gene Expression Regulation*
  • Heart Transplantation
  • Humans
  • Male
  • Mice
  • Mice, Knockout
  • Middle Aged
  • Myocardium / cytology
  • Phosphorylation / genetics
  • Phosphorylation / physiology
  • Sampling Studies
  • Sensitivity and Specificity

Substances

  • Cofilin 2

Supplementary concepts

  • Idiopathic dilation cardiomyopathy