Vascular Cognitive Impairment Linked to Brain Endothelium Inflammation in Early Stages of Heart Failure in Mice

J Am Heart Assoc. 2018 Mar 26;7(7):e007694. doi: 10.1161/JAHA.117.007694.

Abstract

Background: Although advanced heart failure (HF) is a clinically documented risk factor for vascular cognitive impairment, the occurrence and pathomechanisms of vascular cognitive impairment in early stages of HF are equivocal. Here, we characterize vascular cognitive impairment in the early stages of HF development and assess whether cerebral hypoperfusion or prothrombotic conditions are involved.

Methods and results: Tgαq*44 mice with slowly developing isolated HF triggered by cardiomyocyte-specific overexpression of G-αq*44 protein were studied before the end-stage HF, at the ages of 3, 6, and 10 months: before left ventricle dysfunction; at the stage of early left ventricle diastolic dysfunction (with preserved ejection fraction); and left ventricle diastolic/systolic dysfunction, respectively. In 6- to 10-month-old but not in 3-month-old Tgαq*44 mice, behavioral and cognitive impairment was identified with compromised blood-brain barrier permeability, most significantly in brain cortex, that was associated with myelin sheet loss and changes in astrocytes and microglia. Brain endothelial cells displayed increased E-selectin immunoreactivity, which was accompanied by increased amyloid-β1-42 accumulation in piriform cortex and increased cortical oxidative stress (8-OHdG immunoreactivity). Resting cerebral blood flow measured by magnetic resonance imaging in vivo was preserved, but ex vivo NO-dependent cortical arteriole flow regulation was impaired. Platelet hyperreactivity was present in 3- to 10-month-old Tgαq*44 mice, but it was not associated with increased platelet-dependent thrombogenicity.

Conclusions: We report for the first time that vascular cognitive impairment is already present in the early stage of HF development, even before left ventricle systolic dysfunction. The underlying pathomechanism, independent of brain hypoperfusion, involves preceding platelet hyperreactivity and brain endothelium inflammatory activation.

Keywords: blood‐brain barrier; cognitive impairment; endothelium; heart failure; platelet.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyloid beta-Peptides / metabolism
  • Animals
  • Behavior, Animal*
  • Blood Platelets / metabolism
  • Blood-Brain Barrier / metabolism
  • Blood-Brain Barrier / physiopathology
  • Brain / blood supply*
  • Capillary Permeability
  • Cerebral Arteries / metabolism
  • Cerebral Arteries / physiopathology*
  • Cerebrovascular Circulation
  • Cognition
  • Cognition Disorders / etiology*
  • Cognition Disorders / metabolism
  • Cognition Disorders / physiopathology
  • Cognition Disorders / psychology
  • Dementia, Vascular / etiology*
  • Dementia, Vascular / metabolism
  • Dementia, Vascular / physiopathology
  • Dementia, Vascular / psychology
  • Disease Models, Animal
  • Disease Progression
  • Encephalitis / etiology*
  • Encephalitis / metabolism
  • Encephalitis / pathology
  • Encephalitis / physiopathology
  • Endothelium, Vascular / metabolism
  • Endothelium, Vascular / physiopathology*
  • Female
  • GTP-Binding Protein alpha Subunits, Gq-G11 / genetics
  • Genetic Predisposition to Disease
  • Heart Failure / complications*
  • Heart Failure / genetics
  • Heart Failure / metabolism
  • Heart Failure / physiopathology
  • Mice, Transgenic
  • Myocytes, Cardiac / metabolism
  • Peptide Fragments / metabolism
  • Phenotype
  • Time Factors
  • Ventricular Dysfunction, Left / etiology
  • Ventricular Dysfunction, Left / physiopathology
  • Ventricular Function, Left

Substances

  • Amyloid beta-Peptides
  • Peptide Fragments
  • amyloid beta-protein (1-42)
  • GTP-Binding Protein alpha Subunits, Gq-G11