Elevated circulating amyloid concentrations in obesity and diabetes promote vascular dysfunction

J Clin Invest. 2020 Aug 3;130(8):4104-4117. doi: 10.1172/JCI122237.

Abstract

Diabetes, obesity, and Alzheimer's disease (AD) are associated with vascular complications and impaired nitric oxide (NO) production. Furthermore, increased β-site amyloid precursor protein-cleaving (APP-cleaving) enzyme 1 (BACE1), APP, and β-amyloid (Aβ) are linked with vascular disease development and increased BACE1 and Aβ accompany hyperglycemia and hyperlipidemia. However, the causal relationship between obesity and diabetes, increased Aβ, and vascular dysfunction is unclear. We report that diet-induced obesity (DIO) in mice increased plasma and vascular Aβ42 that correlated with decreased NO bioavailability, endothelial dysfunction, and increased blood pressure. Genetic or pharmacological reduction of BACE1 activity and Aβ42 prevented and reversed, respectively, these outcomes. In contrast, expression of human mutant APP in mice or Aβ42 infusion into control diet-fed mice to mimic obese levels impaired NO production, vascular relaxation, and raised blood pressure. In humans, increased plasma Aβ42 correlated with diabetes and endothelial dysfunction. Mechanistically, higher Aβ42 reduced endothelial NO synthase (eNOS), cyclic GMP (cGMP), and protein kinase G (PKG) activity independently of diet, whereas endothelin-1 was increased by diet and Aβ42. Lowering Aβ42 reversed the DIO deficit in the eNOS/cGMP/PKG pathway and decreased endothelin-1. Our findings suggest that BACE1 inhibitors may have therapeutic value in the treatment of vascular disease associated with diabetes.

Keywords: Endocrinology; Nitric oxide; Obesity; Vascular Biology; endothelial cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyloid beta-Peptides / blood*
  • Amyloid beta-Peptides / genetics
  • Animals
  • Cyclic GMP-Dependent Protein Kinases / genetics
  • Cyclic GMP-Dependent Protein Kinases / metabolism
  • Diabetes Mellitus / blood*
  • Diabetes Mellitus / genetics
  • Diabetes Mellitus / pathology
  • Diabetic Angiopathies / blood*
  • Diabetic Angiopathies / genetics
  • Diabetic Angiopathies / pathology
  • Female
  • Humans
  • Male
  • Mice
  • Mice, Transgenic
  • Nitric Oxide / blood
  • Nitric Oxide / genetics
  • Nitric Oxide Synthase Type III / genetics
  • Nitric Oxide Synthase Type III / metabolism
  • Obesity / blood*
  • Obesity / genetics
  • Obesity / pathology
  • Peptide Fragments / blood*
  • Peptide Fragments / genetics
  • Signal Transduction*

Substances

  • Amyloid beta-Peptides
  • Peptide Fragments
  • amyloid beta-protein (1-42)
  • Nitric Oxide
  • NOS3 protein, human
  • Nitric Oxide Synthase Type III
  • Nos3 protein, mouse
  • Cyclic GMP-Dependent Protein Kinases