Reducing RBM20 activity improves diastolic dysfunction and cardiac atrophy

J Mol Med (Berl). 2016 Dec;94(12):1349-1358. doi: 10.1007/s00109-016-1483-3. Epub 2016 Nov 26.

Abstract

Impaired diastolic filling is a main contributor to heart failure with preserved ejection fraction (HFpEF), a syndrome with increasing prevalence and no treatment. Both collagen and the giant sarcomeric protein titin determine diastolic function. Since titin's elastic properties can be adjusted physiologically, we evaluated titin-based stiffness as a therapeutic target. We adjusted RBM20-dependent cardiac isoform expression in the titin N2B knockout mouse with increased ventricular stiffness. A ~50 % reduction of RBM20 activity does not only maintain cardiac filling in diastole but also ameliorates cardiac atrophy and thus improves cardiac function in the N2B-deficient heart. Reduced RBM20 activity partially normalized gene expression related to muscle development and fatty acid metabolism. The adaptation of cardiac growth was related to hypertrophy signaling via four-and-a-half lim-domain proteins (FHLs) that translate mechanical input into hypertrophy signals. We provide a novel link between cardiac isoform expression and trophic signaling via FHLs and suggest cardiac splicing as a therapeutic target in diastolic dysfunction.

Key message: Increasing the length of titin isoforms improves ventricular filling in heart disease. FHL proteins are regulated via RBM20 and adapt cardiac growth. RBM20 is a therapeutic target in diastolic dysfunction.

Keywords: Heart failure; Hypertrophy signaling; Mouse models; RNA processing; Therapy.

Publication types

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

MeSH terms

  • Animals
  • Cardiomegaly / genetics
  • Cardiomegaly / metabolism*
  • Cardiomegaly / pathology
  • Collagen / genetics
  • Collagen / metabolism
  • Diastole / physiology
  • Gene Expression Regulation
  • Heart Failure / genetics
  • Heart Failure / metabolism*
  • Heart Failure / pathology
  • Heart Ventricles / metabolism*
  • Heart Ventricles / pathology
  • Humans
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism
  • LIM Domain Proteins / genetics
  • LIM Domain Proteins / metabolism
  • Male
  • Mice
  • Mice, Knockout
  • Muscle Proteins / genetics
  • Muscle Proteins / metabolism
  • Myocardium / metabolism
  • Myocardium / pathology
  • Protein Kinases / deficiency
  • Protein Kinases / genetics*
  • RNA-Binding Proteins / genetics*
  • RNA-Binding Proteins / metabolism
  • Signal Transduction
  • Stroke Volume / physiology

Substances

  • Fhl1 protein, mouse
  • Intracellular Signaling Peptides and Proteins
  • LIM Domain Proteins
  • Muscle Proteins
  • RBM20 protein, mouse
  • RNA-Binding Proteins
  • Collagen
  • Protein Kinases
  • titin protein, mouse