HMGB1 may act via RAGE to promote angiogenesis in the later phase after intracerebral hemorrhage

Neuroscience. 2015 Jun 4:295:39-47. doi: 10.1016/j.neuroscience.2015.03.032. Epub 2015 Mar 23.

Abstract

Following intracerebral hemorrhage (ICH), high-mobility group box 1 protein (HMGB1) may promote vascular remodeling. Whether HMGB1 supports angiogenesis after ICH is unclear, as are the receptors and downstream signaling pathway(s) involved. We used the rat model of collagenase-induced ICH to determine whether HMGB1 acts via the receptor for advanced glycation end-products (RAGE) to upregulate vascular endothelial growth factor (VEGF), a potent mitogen of endothelial cells and key regulator of normal and abnormal angiogenesis in the late phase of injury. At 3d after ICH induction, rats were treated with saline, ethyl pyruvate (EP) or N-benzyl-4-chloro-N-cyclohexylbenzamide (FPS-ZM1). ICH induced the movement of HMGB1 from the nucleus into the cytoplasm. Levels of HMGB1 and RAGE in the ipsilateral striatum increased within a few days of induction and continued to rise for 7-14d afterward. By 14d after induction, levels of VEGF and vessel density were higher than in the Sham group. Administering EP 3 days after ICH induction prevented much of the stroke-induced increases in vessel density and in expression of HMGB1, RAGE, and VEGF. Administering FPS-ZM1 after ICH blocked much of the stroke-induced increases in vessel density and VEGF expression. Our results suggest that after ICH, HMGB1 may upregulate VEGF in the ipsilateral striatum predominantly via RAGE. Hence, targeting the HMGB1/RAGE signaling pathway may help reduce inappropriate angiogenesis after ICH.

Keywords: angiogenesis; high-mobility group box 1; intracerebral hemorrhage; receptor for advanced glycation end-products.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Benzamides / pharmacology
  • Cerebral Hemorrhage / chemically induced
  • Cerebral Hemorrhage / drug therapy
  • Cerebral Hemorrhage / metabolism*
  • Collagenases / toxicity
  • Corpus Striatum / drug effects
  • Corpus Striatum / metabolism
  • Disease Models, Animal
  • Dose-Response Relationship, Drug
  • Drug Administration Schedule
  • Functional Laterality
  • Gene Expression Regulation / drug effects
  • Glial Fibrillary Acidic Protein / metabolism
  • HMGB1 Protein / metabolism*
  • Male
  • Neovascularization, Physiologic / drug effects
  • Neovascularization, Physiologic / physiology*
  • Pyruvates / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Receptor for Advanced Glycation End Products / antagonists & inhibitors
  • Receptor for Advanced Glycation End Products / metabolism*
  • Up-Regulation / drug effects
  • Vascular Endothelial Growth Factor A / metabolism

Substances

  • Benzamides
  • FPS-ZM1
  • Glial Fibrillary Acidic Protein
  • HMGB1 Protein
  • Pyruvates
  • Receptor for Advanced Glycation End Products
  • Vascular Endothelial Growth Factor A
  • ethyl pyruvate
  • Collagenases