Dysfunction of the β2-spectrin-based pathway in human heart failure

Am J Physiol Heart Circ Physiol. 2016 Jun 1;310(11):H1583-91. doi: 10.1152/ajpheart.00875.2015. Epub 2016 Apr 22.

Abstract

β2-Spectrin is critical for integrating membrane and cytoskeletal domains in excitable and nonexcitable cells. The role of β2-spectrin for vertebrate function is illustrated by dysfunction of β2-spectrin-based pathways in disease. Recently, defects in β2-spectrin association with protein partner ankyrin-B were identified in congenital forms of human arrhythmia. However, the role of β2-spectrin in common forms of acquired heart failure and arrhythmia is unknown. We report that β2-spectrin protein levels are significantly altered in human cardiovascular disease as well as in large and small animal cardiovascular disease models. Specifically, β2-spectrin levels were decreased in atrial samples of patients with atrial fibrillation compared with tissue from patients in sinus rhythm. Furthermore, compared with left ventricular samples from nonfailing hearts, β2-spectrin levels were significantly decreased in left ventricle of ischemic- and nonischemic heart failure patients. Left ventricle samples of canine and murine heart failure models confirm reduced β2-spectrin protein levels. Mechanistically, we identify that β2-spectrin levels are tightly regulated by posttranslational mechanisms, namely Ca(2+)- and calpain-dependent proteases. Furthermore, consistent with this data, we observed Ca(2+)- and calpain-dependent loss of β2-spectrin downstream effector proteins, including ankyrin-B in heart. In summary, our findings illustrate that β2-spectrin and downstream molecules are regulated in multiple forms of cardiovascular disease via Ca(2+)- and calpain-dependent proteolysis.

Keywords: arrhythmias/cardiac; cytoskeleton; ion channels.

Publication types

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

MeSH terms

  • Adult
  • Aged
  • Animals
  • Ankyrins / metabolism
  • Atrial Fibrillation / metabolism*
  • Atrial Fibrillation / physiopathology
  • Calcium / metabolism
  • Calpain / metabolism
  • Case-Control Studies
  • Disease Models, Animal
  • Dogs
  • Down-Regulation
  • Female
  • Heart Failure / metabolism*
  • Heart Failure / physiopathology
  • Heart Ventricles / metabolism*
  • Heart Ventricles / physiopathology
  • Humans
  • Male
  • Mice, Inbred C57BL
  • Middle Aged
  • Proteolysis
  • Signal Transduction
  • Spectrin / metabolism*
  • Stroke Volume
  • Ventricular Function, Left

Substances

  • ANK2 protein, human
  • Ankyrins
  • SPTBN2 protein, human
  • SPTBN2 protein, mouse
  • Spectrin
  • Calpain
  • Calcium