Neuroinflammation in Response to Intracerebral Injections of Different HMGB1 Redox Isoforms

J Innate Immun. 2018;10(3):215-227. doi: 10.1159/000487056. Epub 2018 Feb 23.

Abstract

Background: Neuroinflammation triggered by infection or trauma is the cause of central nervous system dysfunction. High-mobility group box 1 protein (HMGB1), released from stressed and dying brain cells, is a potent neuroinflammatory mediator. The proinflammatory functions of HMGB1 are tightly regulated by post-translational redox modifications, and we here investigated detailed neuroinflammatory responses induced by the individual redox isoforms.

Methods: Male Dark Agouti rats received a stereotactic injection of saline, lipopolysaccharide, disulfide HMGB1, or fully reduced HMGB1, and were accessed for blood-brain barrier modifications using magnetic resonance imaging (MRI) and inflammatory responses by immunohistochemistry.

Results and conclusions: Significant blood-brain barrier disruption appeared 24 h after injection of lipopolysaccharide, disulfide HMGB1, or fully reduced HMGB1 compared to controls, as assessed in post-gadolinium T1-weighted MRI images and confirmed by increased uptake of FITC-conjugated dextran. Immunohistochemistry revealed that both HMGB1 isoforms also induced a local production of IL-1β. Additionally, disulfide HMGB1 increased major histocompatibility complex class II expression and apoptosis. Together, the results demonstrate that extracellular, cerebral HMGB1 causes significant blood-brain barrier disruption in a redox-independent manner and activates several components of neuroinflammation. Blocking HMGB1 might potentially improve clinical outcome in conditions such as stroke and traumatic brain injury.

Keywords: Blood-brain barrier; Brain; HMGB1; Neuroinflammation; Redox.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / genetics
  • Blood-Brain Barrier / drug effects
  • Blood-Brain Barrier / metabolism
  • Blood-Brain Barrier / pathology*
  • Dextrans / metabolism
  • Encephalitis / chemically induced
  • Encephalitis / metabolism*
  • Encephalitis / pathology
  • Fluorescein-5-isothiocyanate / analogs & derivatives
  • Fluorescein-5-isothiocyanate / metabolism
  • HMGB1 Protein / administration & dosage
  • HMGB1 Protein / metabolism*
  • HMGB1 Protein / pharmacology
  • Histocompatibility Antigens Class II / metabolism
  • Immunohistochemistry
  • Interleukin-1beta / metabolism
  • Magnetic Resonance Imaging
  • Male
  • Oxidation-Reduction
  • Protein Isoforms
  • Rats

Substances

  • Dextrans
  • HMGB1 Protein
  • Histocompatibility Antigens Class II
  • Interleukin-1beta
  • Protein Isoforms
  • fluorescein isothiocyanate dextran
  • Fluorescein-5-isothiocyanate