SGLT2 inhibition reduces atherosclerosis by enhancing lipoprotein clearance in Ldlr-/- type 1 diabetic mice

Atherosclerosis. 2018 Apr:271:166-176. doi: 10.1016/j.atherosclerosis.2018.02.028. Epub 2018 Mar 2.

Abstract

Background and aims: Leukocytosis, particularly monocytosis, has been shown to promote atherosclerosis in both diabetic and non-diabetic mouse models. We previously showed that hyperglycemia independently promotes monocytosis and impairs the resolution of atherosclerosis. Since patients with chronic diabetes often develop dyslipidemia and also have increased risk for atherosclerosis, we sought to examine how controlling blood glucose affects atherosclerosis development in the presence of severe hyperlipidemia.

Methods: Diabetes was induced using streptozotocin (STZ) in low density lipoprotein receptor (Ldlr) knockout (Ldlr-/-) mice after which they were fed a high-cholesterol diet for 4 weeks. Control and diabetic mice were treated with vehicle or sodium glucose cotransporter inhibitor (SGLT2i, Phlorizin or Dapagliflozin) for the duration of the diet.

Results: Induction of diabetes resulted in a dramatic increase in plasma cholesterol (TC) and triglyceride (TG) levels. These mice also exhibited an increased number of circulating monocytes and neutrophils. Monocytosis was driven by increased proliferation of progenitor cells in the bone marrow. Tighter glycemic control by SGLT2i treatment not only reduced monocytosis and atherosclerosis but also improved plasma lipoprotein profile. Interestingly, improved lipoprotein profile was not due to decreased TG synthesis or clearance via low density lipoprotein receptor-related protein (Lrp) 1 or scavenger receptor class B member (Scarb1) pathways, but likely mediated by heparin sulfate proteoglycans (HSPG)-dependent clearance mechanisms in the liver. Further examination of the liver revealed an important role for bile acid transporters (Abcg5, Abcg8) and cytochrome P450 enzymes in the clearance of hepatic cholesterol.

Conclusions: These data suggest that tighter glycemic control in diabetes can improve lipoprotein clearance exclusive of Ldlr, likely via HSPG and bile acid pathways, and has an overall net positive effect on atherosclerosis.

Keywords: Atherosclerosis; Dyslipidemia; Hyperglycemia; Lipoproteins; Myelopoiesis; Strepzotocin.

Publication types

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

MeSH terms

  • ATP Binding Cassette Transporter, Subfamily G, Member 5 / metabolism
  • ATP Binding Cassette Transporter, Subfamily G, Member 8 / metabolism
  • Animals
  • Atherosclerosis / blood
  • Atherosclerosis / genetics
  • Atherosclerosis / pathology
  • Atherosclerosis / prevention & control*
  • Benzhydryl Compounds / pharmacology*
  • Biomarkers / blood
  • Blood Glucose / drug effects
  • Blood Glucose / metabolism
  • Cholesterol, Dietary
  • Cytochrome P-450 Enzyme System / metabolism
  • Diabetes Mellitus, Experimental / blood
  • Diabetes Mellitus, Experimental / chemically induced
  • Diabetes Mellitus, Experimental / drug therapy*
  • Diabetes Mellitus, Type 1 / blood
  • Diabetes Mellitus, Type 1 / chemically induced
  • Diabetes Mellitus, Type 1 / drug therapy*
  • Glucosides / pharmacology*
  • Heparin / analogs & derivatives
  • Heparin / metabolism
  • Hyperlipidemias / blood
  • Hyperlipidemias / drug therapy*
  • Hyperlipidemias / genetics
  • Lipoproteins / blood*
  • Lipoproteins / metabolism
  • Liver / drug effects
  • Liver / metabolism
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Monocytes / drug effects
  • Monocytes / metabolism
  • Phlorhizin / pharmacology*
  • Proteoglycans / metabolism
  • Receptors, LDL / deficiency*
  • Receptors, LDL / genetics
  • Sodium-Glucose Transporter 2 Inhibitors / pharmacology*
  • Streptozocin

Substances

  • ABCG5 protein, mouse
  • ABCG8 protein, mouse
  • ATP Binding Cassette Transporter, Subfamily G, Member 5
  • ATP Binding Cassette Transporter, Subfamily G, Member 8
  • Benzhydryl Compounds
  • Biomarkers
  • Blood Glucose
  • Cholesterol, Dietary
  • Glucosides
  • Lipoproteins
  • Proteoglycans
  • Receptors, LDL
  • Sodium-Glucose Transporter 2 Inhibitors
  • heparin proteoglycan
  • dapagliflozin
  • Streptozocin
  • Heparin
  • Cytochrome P-450 Enzyme System
  • Phlorhizin