A cell-penetrating phospholamban-specific RNA aptamer enhances Ca2+ transients and contractile function in cardiomyocytes

J Mol Cell Cardiol. 2014 Nov:76:177-85. doi: 10.1016/j.yjmcc.2014.09.006. Epub 2014 Sep 20.

Abstract

The sarco(endo)plasmic reticulum Ca(2+)-ATPase 2a (SERCA2a)-phospholamban (PLN) system of sarcoplasmic reticulum plays a pivotal role in regulation of intracellular Ca(2+) cycling in ventricular cardiomyocytes. Given that Ca(2+) cycling is impaired in heart failure, proteins that contribute to this process are potential targets for the treatment of this condition. We have now isolated PLN-specific aptamers with a phosphorothioate-modified backbone from a library of RNA molecules containing a randomized 40-nucleotide sequence by application of the systematic evolution of ligands by exponential enrichment (SELEX) protocol with a fusion protein containing the cytoplasmic region of human PLN. One of these aptamers was shortened to a 30-nucleotide oligomer (RNA-Apt30) without loss of function. RNA-Apt30 showed a high affinity for the cytoplasmic region of PLN (Kd=11 nM), but it did not bind to the phosphorylated form of PLN or to a phosphomimetic mutant. It also increased SERCA2a activity in isolated cardiac SR vesicles with an EC50 of 18 nM by relieving PLN-mediated inhibition. Conjugation of RNA-Apt30 to a cell-penetrating peptide allowed its delivery into adult rat cardiomyocytes, in which it enhanced both Ca(2+) transients and contractile function. These effects of the aptamer were also apparent in the presence of the β-adrenergic receptor antagonist propranolol. This cell-penetrating PLN aptamer may thus provide a basis for the development of new therapeutic agents for heart failure without the need for gene transfer or a change in endogenous protein expression.

Keywords: Aptamer; Calcium signaling; Cardiac sarcoplasmic reticulum; Cardiomyocyte; Cell-penetrating peptide; Phospholamban.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aptamers, Nucleotide / chemistry
  • Aptamers, Nucleotide / pharmacology*
  • Base Sequence
  • Calcium Signaling / drug effects*
  • Calcium-Binding Proteins / chemistry
  • Calcium-Binding Proteins / metabolism*
  • Cell-Penetrating Peptides / chemistry
  • Cell-Penetrating Peptides / pharmacology*
  • Cells, Cultured
  • Dogs
  • Male
  • Molecular Sequence Data
  • Myocardial Contraction
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / physiology*
  • Protein Binding
  • Rabbits
  • Rats, Wistar
  • Sarcoplasmic Reticulum / metabolism
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases / metabolism

Substances

  • Aptamers, Nucleotide
  • Calcium-Binding Proteins
  • Cell-Penetrating Peptides
  • phospholamban
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases