Blast exposure elicits blood-brain barrier disruption and repair mediated by tight junction integrity and nitric oxide dependent processes

Sci Rep. 2018 Jul 27;8(1):11344. doi: 10.1038/s41598-018-29341-6.

Abstract

Mild blast-induced traumatic brain injury (TBI) is associated with blood-brain barrier (BBB) disruption. However, the mechanisms whereby blast disrupts BBB integrity are not well understood. To address this issue BBB permeability to peripherally injected 14C-sucrose and 99mTc-albumin was quantified in ten brain regions at time points ranging from 0.25 to 72 hours. In mice, repetitive (2X) blast provoked BBB permeability to 14C-sucrose that persisted in specific brain regions from 0.25 to 72 hours. However, 99mTc-albumin revealed biphasic BBB disruption (open-closed-open) over the same interval, which was most pronounced in frontal cortex and hippocampus. This indicates that blast initiates interacting BBB disruption and reparative processes in specific brain regions. Further investigation of delayed (72 hour) BBB disruption revealed that claudin-5 (CLD5) expression was disrupted specifically in the hippocampus, but not in dorsal striatum, a brain region that showed no blast-induced BBB permeability to sucrose or albumin. In addition, we found that delayed BBB permeability and disrupted CLD5 expression were blocked by the nitric oxide synthase inhibitor N(G)-nitro-L-arginine methyl ester (L-NAME). These data argue that latent nitric oxide-dependent signaling pathways initiate processes that result in delayed BBB disruption, which are manifested in a brain-region specific manner.

Publication types

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

MeSH terms

  • Albumins / metabolism
  • Animals
  • Blast Injuries / metabolism*
  • Blast Injuries / pathology*
  • Blood-Brain Barrier / drug effects
  • Blood-Brain Barrier / pathology*
  • Brain Injuries, Traumatic / metabolism
  • Brain Injuries, Traumatic / pathology
  • Carbon Radioisotopes
  • Claudin-5 / metabolism
  • Cyclooxygenase Inhibitors / pharmacology
  • Gliosis / pathology
  • Male
  • Mice, Inbred C57BL
  • NG-Nitroarginine Methyl Ester / pharmacology
  • Nitric Oxide / metabolism*
  • Nitric Oxide Synthase / antagonists & inhibitors
  • Nitric Oxide Synthase / metabolism
  • Organ Specificity
  • Permeability
  • Radiopharmaceuticals / metabolism
  • Sucrose / metabolism
  • Tight Junctions / drug effects
  • Tight Junctions / metabolism*
  • Time Factors
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Albumins
  • Carbon Radioisotopes
  • Claudin-5
  • Cyclooxygenase Inhibitors
  • Radiopharmaceuticals
  • Tumor Necrosis Factor-alpha
  • Nitric Oxide
  • Sucrose
  • Carbon-14
  • Nitric Oxide Synthase
  • NG-Nitroarginine Methyl Ester