Role of angiopoietin-like protein 3 in sugar-induced dyslipidemia in rhesus macaques: suppression by fish oil or RNAi

J Lipid Res. 2020 Mar;61(3):376-386. doi: 10.1194/jlr.RA119000423. Epub 2020 Jan 9.

Abstract

Angiopoietin-like protein 3 (ANGPTL3) inhibits lipid clearance and is a promising target for managing cardiovascular disease. Here we investigated the effects of a high-sugar (high-fructose) diet on circulating ANGPTL3 concentrations in rhesus macaques. Plasma ANGPTL3 concentrations increased ∼30% to 40% after 1 and 3 months of a high-fructose diet (both P < 0.001 vs. baseline). During fructose-induced metabolic dysregulation, plasma ANGPTL3 concentrations were positively correlated with circulating indices of insulin resistance [assessed with fasting insulin and the homeostatic model assessment of insulin resistance (HOMA-IR)], hypertriglyceridemia, adiposity (assessed as leptin), and systemic inflammation [C-reactive peptide (CRP)] and negatively correlated with plasma levels of the insulin-sensitizing hormone adropin. Multiple regression analyses identified a strong association between circulating APOC3 and ANGPTL3 concentrations. Higher baseline plasma levels of both ANGPTL3 and APOC3 were associated with an increased risk for fructose-induced insulin resistance. Fish oil previously shown to prevent insulin resistance and hypertriglyceridemia in this model prevented increases of ANGPTL3 without affecting systemic inflammation (increased plasma CRP and interleukin-6 concentrations). ANGPTL3 RNAi lowered plasma concentrations of ANGPTL3, triglycerides (TGs), VLDL-C, APOC3, and APOE. These decreases were consistent with a reduced risk of atherosclerosis. In summary, dietary sugar-induced increases of circulating ANGPTL3 concentrations after metabolic dysregulation correlated positively with leptin levels, HOMA-IR, and dyslipidemia. Targeting ANGPTL3 expression with RNAi inhibited dyslipidemia by lowering plasma TGs, VLDL-C, APOC3, and APOE levels in rhesus macaques.

Keywords: C-reactive protein; RNA interference; apolipoproteins; inflammation; insulin resistance; lipoproteins; metabolic disorders; nonhuman primate; triglycerides.

Publication types

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

MeSH terms

  • Angiopoietin-like Proteins / antagonists & inhibitors*
  • Angiopoietin-like Proteins / blood
  • Angiopoietin-like Proteins / metabolism
  • Animals
  • Dietary Supplements
  • Dyslipidemias / blood
  • Dyslipidemias / chemically induced
  • Dyslipidemias / drug therapy*
  • Fish Oils / administration & dosage
  • Fish Oils / pharmacology*
  • Fructose / antagonists & inhibitors*
  • Inflammation / metabolism
  • Lipoproteins / metabolism
  • Macaca mulatta
  • Male
  • RNA Interference*

Substances

  • Angiopoietin-like Proteins
  • Fish Oils
  • Lipoproteins
  • Fructose