Blood-brain barrier disruption induced by hemoglobin in vivo: Involvement of up-regulation of nitric oxide synthase and peroxynitrite formation

Brain Res. 2014 Jul 7:1571:25-38. doi: 10.1016/j.brainres.2014.04.042. Epub 2014 May 9.

Abstract

Accumulating evidence has demonstrated that up-regulation of nitric oxide synthase (NOS) and subsequent peroxynitrite (ONOO(-)) formation exert a devastating effect on the damage of BBB in multiple diseases. However, considerably less attention has been focused on the role of NOS/ONOO(-) in BBB disruption after intracerebral hemorrhage (ICH). Using an experimental stroke model by injecting hemoglobin (Hb) into the caudate nucleus of male Sprague Dawley rats, we explored the role of NOS/ONOO(-) in BBB disruption after ICH. Brain edema content, behavioral changes, alterations of TJ proteins (claudin-5 and ZO-1), expression of neuronal NOS (nNOS), inducible NOS (iNOS) and endothelial NOS (eNOS), formation of 3-nitrotyrosine (3-NT), as well as NO production were investigated. Hb in the rat brain led to a significant brain edema production and neurological deficits. Overexpressed NOS was concomitant with large quantities of 3-NT formation. Moreover, sites of enhanced nNOS, iNOS, eNOS and 3-NT immunoreactivity were colocalized with diminished or discontinuous ZO-1 and/or claudin-5 staining as evidenced by Western blot and immunofluorescence, indicating the involvement of NOS and ONOO(-) in the BBB disruption. Meaningfully, levels of 3-NT in serum, which had a similar tendency with that of in brain tissues (r=0.934, P<0.001), had a marked correlation with brain edema content (r=0.782, P<0.001) and neurological deficits (r=0.851, P<0.001). We concluded that ONOO(-) formation by the upregulation of NOS may play a central role in promoting the BBB damage following ICH. Moreover, ONOO(-) may be a promising biomarker for the judgment or prediction of brain injury and clinical prognosis after ICH.

Keywords: Blood–brain barrier; Brain edema; Hemoglobin; Intracerebral hemorrhage; Nitric oxide synthase; Peroxynitrite.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Analysis of Variance
  • Animals
  • Blood-Brain Barrier / drug effects*
  • Blood-Brain Barrier / physiopathology
  • Brain Edema / metabolism
  • Cerebral Hemorrhage / chemically induced*
  • Cerebral Hemorrhage / pathology*
  • Claudin-5 / metabolism
  • Disease Models, Animal
  • Enzyme-Linked Immunosorbent Assay
  • Hemoglobins / toxicity*
  • Male
  • Motor Activity / drug effects
  • Nitric Oxide / blood
  • Nitric Oxide Synthase / metabolism*
  • Peroxynitrous Acid / metabolism*
  • Rats
  • Rats, Sprague-Dawley
  • Time Factors
  • Tyrosine / analogs & derivatives
  • Tyrosine / metabolism
  • Up-Regulation / drug effects*
  • Zonula Occludens-1 Protein / metabolism

Substances

  • Claudin-5
  • Cldn5 protein, rat
  • Hemoglobins
  • Tjp1 protein, rat
  • Zonula Occludens-1 Protein
  • Peroxynitrous Acid
  • Nitric Oxide
  • 3-nitrotyrosine
  • Tyrosine
  • Nitric Oxide Synthase