Lethal Arrhythmogenic Role of Left Ventricular Myocardial Interstitial Fibrosis in Apolipoprotein E/Low-Density Lipoprotein Receptor Double-Knockout Mice with Metabolic Dysfunction-Associated Steatohepatitis

Int J Mol Sci. 2024 Dec 27;26(1):144. doi: 10.3390/ijms26010144.

Abstract

The combination of alcohol and a low-carbohydrate, high-protein, high-fat atherogenic diet (AD) increases the risk of lethal arrhythmias in apolipoprotein E/low-density lipoprotein receptor double-knockout (AL) mice with metabolic dysfunction-associated steatotic liver disease (MASLD). This study investigates whether left ventricular (LV) myocardial interstitial fibrosis (MIF), formed during the progression of metabolic dysfunction-associated steatohepatitis (MASH), contributes to this increased risk. Male AL mice were fed an AD with or without ethanol for 16 weeks, while age-matched AL and wild-type mice served as controls. Liver and heart tissues were analyzed, and susceptibility to lethal arrhythmias was assessed through histopathology, fluorescence immunohistochemistry, RNA-Seq, RT-PCR, and lethal arrhythmia-evoked test. Ethanol combined with an AD significantly induced LV MIF in MASH-affected AL mice, as shown by increased fibrosis-related gene expression, Sirius-Red staining, and elevated collagen 1a1 and 3a1 mRNA levels, alongside a higher incidence of lethal arrhythmias. Cardiac myofibroblasts exhibited sympathetic activation and produced elevated levels of fibrosis-promoting factors. This study highlights the role of cardiac myofibroblasts in LV MIF, contributing to an increased incidence of lethal arrhythmias in MASH-affected AL mice fed ethanol and AD, even after the alcohol was fully metabolized on the day of consumption.

Keywords: alcohol; high-fat atherogenic diet; high-protein; left ventricular myocardial interstitial fibrosis; lethal arrhythmia; low-carbohydrate; metabolic dysfunction-associated steatotic liver disease.

MeSH terms

  • Animals
  • Apolipoproteins E* / deficiency
  • Apolipoproteins E* / genetics
  • Apolipoproteins E* / metabolism
  • Arrhythmias, Cardiac* / etiology
  • Arrhythmias, Cardiac* / genetics
  • Arrhythmias, Cardiac* / metabolism
  • Arrhythmias, Cardiac* / pathology
  • Diet, High-Fat / adverse effects
  • Disease Models, Animal
  • Fatty Liver / etiology
  • Fatty Liver / genetics
  • Fatty Liver / metabolism
  • Fatty Liver / pathology
  • Fibrosis*
  • Heart Ventricles / metabolism
  • Heart Ventricles / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • Myocardium* / metabolism
  • Myocardium* / pathology
  • Myofibroblasts / metabolism
  • Myofibroblasts / pathology
  • Receptors, LDL / deficiency
  • Receptors, LDL / genetics
  • Receptors, LDL / metabolism

Substances

  • Apolipoproteins E
  • Receptors, LDL