Fibrillin-1 impairment enhances blood-brain barrier permeability and xanthoma formation in brains of apolipoprotein E-deficient mice

Neuroscience. 2015 Jun 4:295:11-22. doi: 10.1016/j.neuroscience.2015.03.023. Epub 2015 Mar 19.

Abstract

We recently reported that apolipoprotein E (ApoE)-deficient mice with a mutation in the fibrillin-1 gene (ApoE(-/-)Fbn1(C1039G+/-)) develop accelerated atherosclerosis with enhanced inflammation, atherosclerotic plaque rupture, myocardial infarction and sudden death. In the brain, fibrillin-1 functions as an attachment protein in the basement membrane, providing structural support to the blood-brain barrier (BBB). Here, we investigated whether fibrillin-1 impairment affects the permeability of the BBB proper and the blood-cerebrospinal fluid barrier (BCSFB), and whether this leads to the accelerated accumulation of lipids (xanthomas) in the brain. ApoE(-/-) (n=61) and ApoE(-/-)Fbn1(C1039G+/-) (n=73) mice were fed a Western-type diet (WD). After 14 weeks WD, a significantly higher permeability of the BBB was observed in ApoE(-/-)Fbn1(C1039G+/-) mice compared to age-matched ApoE(-/-) mice. This was accompanied by leukocyte infiltration, enhanced expression of pro-inflammatory cytokines, matrix metalloproteinases and transforming growth factor-β, and by decreased expression of tight junction proteins claudin-5 and occludin. After 20 weeks WD, 83% of ApoE(-/-)Fbn1(C1039G+/-) mice showed xanthomas in the brain, compared to 23% of their ApoE(-/-) littermates. Xanthomas were mainly located in fibrillin-1-rich regions, such as the choroid plexus and the neocortex. Our findings demonstrate that dysfunctional fibrillin-1 impairs BBB/BCSFB integrity, facilitating peripheral leukocyte infiltration, which further degrades the BBB/BCSFB. As a consequence, lipoproteins can enter the brain, resulting in accelerated formation of xanthomas.

Keywords: blood–brain barrier; choroid plexus; fibrillin-1; xanthomas.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acrylamides / metabolism
  • Animals
  • Apolipoproteins E / deficiency*
  • Apolipoproteins E / genetics
  • Blood-Brain Barrier / physiopathology*
  • Blood-Brain Barrier / ultrastructure
  • Brain / pathology*
  • Brain Diseases / pathology*
  • Cytokines / metabolism
  • Disease Models, Animal
  • Female
  • Fibrillin-1
  • Fibrillins
  • Gadolinium / pharmacokinetics
  • Magnetic Resonance Imaging
  • Male
  • Mice
  • Mice, Transgenic
  • Microfilament Proteins / genetics
  • Microfilament Proteins / metabolism*
  • Microscopy, Electron, Transmission
  • Nerve Tissue Proteins / metabolism
  • Permeability
  • Vascular Cell Adhesion Molecule-1 / metabolism
  • Xanthomatosis / genetics
  • Xanthomatosis / pathology*
  • beta-Alanine / analogs & derivatives
  • beta-Alanine / metabolism

Substances

  • 2-(2,6-dichloro-4-((3-furan-2-ylacryloylamino)methyl)benzoylamino)-3-((thiazolidine-4-carbonyl)amino)propionic acid
  • Acrylamides
  • Apolipoproteins E
  • Cytokines
  • Fbn1 protein, mouse
  • Fibrillin-1
  • Fibrillins
  • Microfilament Proteins
  • Nerve Tissue Proteins
  • Vascular Cell Adhesion Molecule-1
  • beta-Alanine
  • Gadolinium