Low density lipoproteins promote unstable calcium handling accompanied by reduced SERCA2 and connexin-40 expression in cardiomyocytes

PLoS One. 2013;8(3):e58128. doi: 10.1371/journal.pone.0058128. Epub 2013 Mar 13.

Abstract

The damaging effects of high plasma levels of cholesterol in the cardiovascular system are widely known, but little attention has been paid to direct effects on cardiomyocyte function. We therefore aimed at testing the hypothesis that Low Density Lipoprotein (LDL) cholesterol affects calcium dynamics and signal propagation in cultured atrial myocytes. For this purpose, mRNA and protein expression levels were determined by real time PCR and western blot analysis, respectively, and intracellular calcium was visualized in fluo-4 loaded atrial HL-1 myocyte cultures subjected to field stimulation. At low stimulation frequencies all cultures had uniform calcium transients at all tested LDL concentrations. However, 500 µg LDL/mL maximally reduced the calcium transient amplitude by 43% from 0.30 ± 0.04 to 0.17 ± 0.02 (p<0.05). Moreover, LDL-cholesterol dose-dependently increased the fraction of alternating and irregular beat-to-beat responses observed when the stimulation interval was shortened. This effect was linked to a concurrent reduction in SERCA2, RyR2, IP3RI and IP3RII mRNA levels. SERCA2 protein levels were also reduced by 43% at 200 µg LDL/mL (p<0.05) and SR calcium loading was reduced by 38 ± 6% (p<0.001). By contrast, HDL-cholesterol had no significant effect on SERCA expression or SR calcium loading. LDL-cholesterol also slowed the conduction velocity of the calcium signal from 3.2+0.2 mm/s without LDL to 1.7 ± 0.1 mm/s with 500 µg LDL/mL (p<0.05). This coincided with a reduction in Cx40 expression (by 44 ± 3%; p<0.05 for mRNA and by 79 ± 2%; p<0.05 for Cx40 protein at 200 µg/ml LDL) whereas the Cx-43 expression did not significantly change. In conclusion, LDL-cholesterol destabilizes calcium handling in cultured atrial myocytes subjected to rapid pacing by reducing SERCA2 and Cx40 expression and by slowing the conduction velocity of the calcium signal.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium / metabolism*
  • Calcium Signaling / drug effects
  • Cell Line
  • Cholesterol Esters / metabolism
  • Cholesterol, LDL / metabolism
  • Connexins / genetics*
  • Connexins / metabolism
  • Gap Junction alpha-5 Protein
  • Gene Expression Regulation* / drug effects
  • Humans
  • Intracellular Space / metabolism
  • Lipoproteins, LDL / metabolism*
  • Lipoproteins, LDL / pharmacology
  • Mice
  • Myocytes, Cardiac / metabolism*
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases / genetics*
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases / metabolism

Substances

  • Cholesterol Esters
  • Cholesterol, LDL
  • Connexins
  • Lipoproteins, LDL
  • Sarcoplasmic Reticulum Calcium-Transporting ATPases
  • Calcium

Grants and funding

This work was supported by grants from the Spanish Ministry of Science and Innovation: SAF2011-30312 and CNIC2009-08 to Leif Hove Madsen, DPI2009-06999 to Raúl Benítez and from the Spanish Ministry of Health and Consume: FIS PI11/00747 to Vicenta Llorente. Funding from Redes de Investigación Cooperativa, Instituto de Salud Carlos III, red REDINSCOR RD06-0003-0000 and RD06-0003-0015 is also acknowledged. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.